\documentclass[10pt]{article}

\usepackage{fullpage}
\usepackage{setspace}
\usepackage{parskip}
\usepackage{titlesec}
\usepackage[section]{placeins}
\usepackage{xcolor}
\usepackage{breakcites}
\usepackage{lineno}
\usepackage{hyphenat}





\PassOptionsToPackage{hyphens}{url}
\usepackage[colorlinks = true,
            linkcolor = blue,
            urlcolor  = blue,
            citecolor = blue,
            anchorcolor = blue]{hyperref}
\usepackage{etoolbox}
\makeatletter
\patchcmd\@combinedblfloats{\box\@outputbox}{\unvbox\@outputbox}{}{%
  \errmessage{\noexpand\@combinedblfloats could not be patched}%
}%
\makeatother


\usepackage{natbib}




\renewenvironment{abstract}
  {{\bfseries\noindent{\abstractname}\par\nobreak}\footnotesize}
  {\bigskip}

\titlespacing{\section}{0pt}{*3}{*1}
\titlespacing{\subsection}{0pt}{*2}{*0.5}
\titlespacing{\subsubsection}{0pt}{*1.5}{0pt}


\usepackage{authblk}


\usepackage{graphicx}
\usepackage[space]{grffile}
\usepackage{latexsym}
\usepackage{textcomp}
\usepackage{longtable}
\usepackage{tabulary}
\usepackage{booktabs,array,multirow}
\usepackage{amsfonts,amsmath,amssymb}
\providecommand\citet{\cite}
\providecommand\citep{\cite}
\providecommand\citealt{\cite}
% You can conditionalize code for latexml or normal latex using this.
\newif\iflatexml\latexmlfalse
\providecommand{\tightlist}{\setlength{\itemsep}{0pt}\setlength{\parskip}{0pt}}%

\AtBeginDocument{\DeclareGraphicsExtensions{.pdf,.PDF,.eps,.EPS,.png,.PNG,.tif,.TIF,.jpg,.JPG,.jpeg,.JPEG}}

\usepackage[utf8]{inputenc}
\usepackage[T2A]{fontenc}
\usepackage[polish,ngerman,greek,english]{babel}



\usepackage{float}








\begin{document}

\title{Tailoring beneficial microbe-plant interactions for ``one health'',
benefits}



\author[1]{Christine Foyer}%
\author[2]{Ashish Srivastava}%
\author[2]{Reema D. Singh}%
\author[3]{Girdhar  Pandey}%
\author[2]{Prasun K. Mukherjee}%
\affil[1]{University of Birmingham School of Biosciences}%
\affil[2]{Bhabha Atomic Research Centre Technical Physics Division}%
\affil[3]{University of Delhi Department of Plant Molecular Biology}%


\vspace{-1em}



  
  \date{May 18, 2024}


\begingroup
\let\center\flushleft
\let\endcenter\endflushleft
\maketitle
\endgroup





\selectlanguage{english}
\begin{abstract}
Plants are an intrinsic part of the soil community and the ``one health
concept'' considers that human health is intimately connected to the
health of animals, plants, and microbial environments. Plant-microbe
interactions are a cornerstone of one health, the soil microbiome being
comprised of a diverse range of organisms, interacts in the rhizosphere
through continuous molecular communications. Soils are a source and
reservoir of pathogens, as well as beneficial microorganisms. Hence, the
molecular dialogue at the rhizosphere interface is crucial not only for
successful plant-microbe interactions but also for crop resilience and
stress tolerance. The plant-microbe continuum forms a network of
underground ``nutrient highways'' that benefit both plant and microbial
communities. It also serves as a significant sink for atmospheric CO
\textsubscript{2}. While microbial diversity is generally positively
associated with one health, the host range of beneficial microbes
currently limits their successful exploitation with a wide range of
microbial communities. We consider the possibility of increasing the
host range of beneficial microbes, including arbuscular mycorrhiza fungi
(AMF) and rhizobia, and how current genetic incompatibility and/or
activation of robust plant defenses, can be overcome while accepting
that significant challenges exist in translating laboratory findings
into the field. We consider why AMF inoculants and plant
growth-promoting microbes are not always beneficial under field
conditions and suggest possible approaches for tailoring plant-microbe
interactions to assist plant breeding efforts in crop resilience.%
\end{abstract}%



\sloppy


\textbf{Tailoring beneficial microbe-plant interactions for ``one
health'', benefits}

Ashish K. Srivastava\textsuperscript{1,2*}, Reema D.
Singh\textsuperscript{1}, Girdhar K. Pandey\textsuperscript{3}, Prasun
K. Mukherjee\textsuperscript{1,2}, Christine H.
Foyer\textsuperscript{4*}

\textsuperscript{1}Nuclear Agriculture and Biotechnology Division,
Bhabha Atomic Research Centre, Mumbai, Maharashtra 400085, India

\textsuperscript{2}HomiBhabha National Institute, Mumbai-400094, India

\textsuperscript{3}Department of Plant Molecular Biology, University of
Delhi South Campus, Benito Juarez Road, Dhaula Kuan, New Delhi-110021,
India

\textsuperscript{4}School of Biosciences, University of Birmingham,
Edgbaston, Birmingham, B15 2TT, UK

*For correspondence:

Christine Helen Foyer (C.H.Foyer@bham.ac.uk)

Ashish Kumar Srivastava (ashishbarc@gmail.com)

\textbf{Keywords:} Atmospheric CO\textsubscript{2} levels, host-range
specificity, microbial transplantation, receptor-ligand signaling, root
microbiome.

\textbf{Abstract}

Plants are an intrinsic part of the soil community and the ``one health
concept'' considers that human health is intimately connected to the
health of animals, plants, and microbial environments. Plant-microbe
interactions are a cornerstone of one health, the soil microbiome being
comprised of a diverse range of organisms, interacts in the rhizosphere
through continuous molecular communications. Soils are a source and
reservoir of pathogens, as well as beneficial microorganisms. Hence, the
molecular dialogue at the rhizosphere interface is crucial not only for
successful plant-microbe interactions but also for crop resilience and
stress tolerance. The plant-microbe continuum forms a network of
underground ``nutrient highways'' that benefit both plant and microbial
communities. It also serves as a significant sink for atmospheric
CO\textsubscript{2}. While microbial diversity is generally positively
associated with one health, the host range of beneficial microbes
currently limits their successful exploitation with a wide range of
microbial communities. We consider the possibility of increasing the
host range of beneficial microbes, including arbuscular mycorrhiza fungi
(AMF) and rhizobia, and how current genetic incompatibility and/or
activation of robust plant defenses, can be overcome while accepting
that significant challenges exist in translating laboratory findings
into the field. We consider why AMF inoculants and plant
growth-promoting microbes are not always beneficial under field
conditions and suggest possible approaches for tailoring plant-microbe
interactions to assist plant breeding efforts in crop resilience.

\emph{}

\textbf{INTRODUCTION}

Soil microbial communities are crucial to the ``one health'' concept
because they connect the health of ecosystems, the microbial communities
associated with plants, animals, and humans (Fig. 1), functioning as a
`second genome' (an `extended genotype' or an `eco-holobiont'). The
microbial communities of different organisms are interconnected in a
manner that influences the fitness and performance of the different
prokaryotic and eukaryotic organisms (Banerjee \& van der Heijden,
2023). Similar functions can be attributed to microbial communities in
the human gut and plant rhizosphere including nutrient uptake,
modulating host immunity, prevention of pathogen colonization, and
improving overall health. Harnessing the second genome for food
production can also lower the environmental impact and residual effect
of chemicals on the food chain because they influence nutrient recycling
and pollutant degradation, thereby increasing crop resilience to climate
variabilities (Trivedi, Batista, Bazany, \& Singh, 2022).

Plants have evolved efficient strategies to avoid infection by microbial
pathogens such as restricting microbe entry and multiplication. However,
plant-microbiome associations go far beyond pathogens, the overall
diversity of microbial symbionts, commensals, and amensals being pivotal
to the overall health of the biosphere. In particular, the root-driven
sequestration of carbon is attributable to the exchange and transport of
nutrients between the roots of perennial plants, particularly trees, and
rhizosphere bacteria and fungi. Soil microbes are the key drivers of
carbon storage in soils, surpassing other soil processes. Since,
microbial carbon use efficiency (CUE) is a major determinant of global
soil organic carbon storage, understanding the plant-microbe
interactions that underpin processes such as CUE can improve
nature-based solutions to climate change.

The plant-microbe community includes a diverse range of endophytes, that
asymptomatically colonize the internal tissues of almost all plants
(endosphere), as well as inhabiting the outside (ectosphere) plant
organs (Ghatak, Chaturvedi, Waldherr, Subbarao, \& Weckwerth, 2023;
Sohrabi, Paasch, Liber, \& He, 2023). The plant-beneficial bacteria
(PBB), arbuscular mycorrhizal fungi (AMF), and plant-growth promoting
microorganisms (PGPM) stimulate plant growth and development under
optimal and stress conditions through a range of mechanisms (Fig. 2).
Rhizosphere establishment and the persistence of beneficial microbes
rely on efficient root colonization wherein they feed on the
carbohydrates and other exudes. In turn, they assist in the uptake of
essential nutrients, particularly nitrogen (N), phosphorus (P) and
potassium (K), and produce phytohormones such as indole-3-acetic acid
(IAA), cytokinins (CK) and gibberellins, and also siderophores and
thereby enhance plant fitness and resilience to environmental stresses
(Bai et al., 2022; Ghatak et al., 2023; Turner, James, \& Poole, 2013),
such as salt (Chakraborty et al., 2021; Li, La, Zhang, Gao, \& Tian,
2021) and drought (Bazany, Wang, Delgado-Baquerizo, Singh, \& Trivedi,
2022; de Vries, Griffiths, Knight, Nicolitch, \& Williams, 2020).

Seed microbiota including epiphytes that inhabit the seed coat and
endophytes that colonize the endosphere, including the embryo,
endosperm, aleurone, and perisperm, are central to plant establishment
(Nelson, 2018; Nelson, Simoneau, Barret, Mitter, \& Compant, 2018). This
microbial community not only pioneers next-generation functions in the
seedling establishment but also facilitates subsequent microbial
colonization from the spermosphere (Fig. 2A). Microbe-assisted solutions
to combat the negative impact of climate change may improve plant
survival, in a world faced with an increased frequency of heat waves,
floods, droughts and contamination of toxic heavy metals. However, a
much deeper understanding of inter-organism communication is required to
tailor the microbial community for maximizing plant growth and
productivity, especially under realistic field scenarios. Building on a
firm foundation of previous reviews on this topic such as Saad et al.
(2020); Ke et al. (2021) and Banerjee \& van der Heijden (2023), we
present a synthesis of current research information, while highlighting
the constraints to practical feasibility.

\textbf{MULTIPLE PATHWAYS FOR INTER-ORGANISM COMMUNICATION}

Microbe-derived bioactive metabolites

Microbe-derived compounds that trigger enhanced plant growth and defense
are therefore attractive and promising alternatives to agricultural
chemicals. In particular, rhizosphere bacteria produce a portfolio of
bioactive secondary metabolites (BSMs) and inhibitory allelochemicals
that are responsible for Induced Systemic Resistance (IR), biocontrol,
and ecological fitness (Fig. 2A). For example, the typical
plant-associated species,\emph{Bacillus velezensis} has considerable
biocontrol potential, based on its ability to trigger IR leading to
rapid and robust defense responses, as well as direct antagonistic
actions on pathogens (Ongena et al., 2007). Over 12\% of the genome in
bacteria such as \emph{B. velezensis} is devoted to the synthesis of
compounds that contribute to ecological competence and biocontrol
activity. They produce a wide range of non-ribosomally synthesized
compounds such as oligopeptides, cyclic lipopeptides (CLPs), and
polyketides (PKs), in addition to post-translationally-modified
lanthipeptides and bacteriocins. These molecules play a key role in
multitrophic interactions because they can be antagonistic with other
microbes and/or beneficial to the host via the stimulation of innate
immune responses leading to IR. BSMs are not only produced \emph{in
vitro} conditions but also \emph{in planta} by bacterial cells evolving
as biofilm-structured microcolonies on root tissues (Andri\selectlanguage{polish}ć \selectlanguage{english}et al.,
2021; Cawoy et al., 2015; Zihalirwa Kulimushi, Arg\selectlanguage{ngerman}üelles Arias, Franzil,
Steels, \& Ongena, 2017).

Plant-associated bacteria have evolved a polymer-sensing system to
perceive the host. They increase BSM synthesis in response to the
perception of root exudates. For example, the production of the cyclic
lipopeptide surfactin by \emph{B. velezensis} ~is stimulated by pectin,
which is recognized as a cell surface molecular pattern in root
exudates. Surfactin, which is synthesized non-ribosomally by a complex
enzyme system, is formed as a mix of naturally coproduced homologs with
fatty acid chains of various lengths (Hoff et al., 2021). It optimizes
biofilm formation, motility, and early root colonization by the
bacterium. It also reinforces the defensive capacity of the host. The IR
phenotypes triggered by surfactin and other PBBs are an attractive
addition to the crop protection toolbox, as bio-sourced alternatives to
chemicals. However, the underlying biochemical and molecular basis for
PBB action remains poorly understood.

Receptor-ligand interaction

The complex and reiterative dialogue between plants and soil
microorganisms involves extensive local and systemic communication
systems that are based, at least in part, on plant receptors that detect
microbe-associated molecular patterns (MAMPs) and pathogen-associated
molecular patterns (PAMPs). These molecules are restricted to pathogens
and are not generally conserved and shared by a wide range of microbes,
trigger IR and play a prominent role in determining the success or
failure of any plant/microbe interaction (Lü, Liu, Yu, Shi, \& Liu,
2022). Chitin, which is a fungal cell wall homopolymer of unbranched
\selectlanguage{greek}β-\selectlanguage{english}1,4-linked N-acetylglucosamine (GlcNAc), is a key MAMP component that
is recognized by~plasma-membrane pattern recognition receptors~(PRRs)
(Lu, Liu, Yu, Shi, \& Liu, 2022). The breakdown products of chitin
(chitooligosaccharides: COs) are perceived by plant lysin motif (LysM)
plasma membrane receptors triggering defence-gene induction, secretion
of chitinases, a plasma membrane-derived oxidative burst and restriction
of fungal growth (Chen et al., 2021; X. He et al., 2021; Morella et al.,
2020; X. Zhou et al., 2022). The secretion of LysM-containing effector
proteins that sequester AMF cell-wall derived COs plays a major role in
the control of chitin-triggered host immunity (Zeng et al., 2020).
Beneficial microbes, including rhizobia and AMF, which inhabit plant
tissues can establish a mutualistic relationship with their hosts by
either evading or suppressing host immunity (Fig. 2). The molecular
dialogue between plant immune system and rhizosphere microbiota not only
promotes colonization by beneficial microbes but it also prevents
growth-defense trade-offs triggered by the MAMP-rich rhizosphere
environment.

Plants secrete a range of chemicals such as flavonoids and
strigolactones that are recognized by symbiotic rhizobia, which in turn
secrete bacterial lipo-chitooligosaccharides~(LCOs or Nod factors) that
have a core structure of three to five N-acetyl glucosamines with an
acyl chain attached to the non-reducing residue (Escudero-Martinez \&
Bulgarelli, 2023). Rhizobium Nod factors that are perceived by legumes
and~\emph{Parasponia} ~species trigger a common symbiotic signaling
(SYM) pathway that involves genes that are also required for AMF
symbiosis (Escudero-Martinez et al., 2022; Oyserman et al., 2022). LCO
receptor has a well-conserved hydrophobic structural signature that
monitors the composition of amphiphilic LCO molecules. Receptor-ligand
interactions provide a kinetic proof-reading mechanism for the selective
recognition-guided activation of symbiotic signaling in legumes,
determining rhizobia-legume compatibility (Gysel et al., 2021).
Rhizobial species either have a broad host range
(e.g.\emph{Sinorhizobium fredii} NGR234 interactions with over 200
distantly related legumes) a narrow host range like \emph{S. meliloti}
that primarily nodulates \emph{M. truncatula} or \emph{M. sativa}
(Kelly, Radutoiu, \& Stougaard, 2017). Many \emph{S. Meliloti} strains
induce incompatible signaling due to two \emph{Nodulation Specificity 1}
locus (\emph{NS1a} and \emph{NS1b} ) genes that encode malectin-like
leucine-rich repeat receptor kinases, which block tissue invasion and
root nodule induction. NS1 activation is dependent upon the bacterial
gene \emph{rns1} (Root nodule symbiosis) that encodes a type I-secreted
protein (Liu et al., 2022).

Unlike the relatively well-characterized interactions between plants,
AMF, and rhizobia, the molecular basis for cooperative interactions
between PBBs and plants remains poorly characterized. Some PBBs display
MAMPs, while others appear to bypass this high-affinity protein
receptor-mediated surveillance system that triggers host immune
responses. These are then recognized by cell-surface receptors, PRRs.
For example, membrane lipid-dependent elicitation by surfactin induces
an atypical early immune response including an intra-cellular burst of
reactive oxygen species (ROS) and low calcium influx that triggers
systemic resistance to \emph{Botrytis cinerea} infection
in\emph{Arabidopsis thaliana} (Pr\selectlanguage{polish}š\selectlanguage{english}i\selectlanguage{polish}ć \selectlanguage{english}et al., 2023; Hoff et al., 2021;
Pr\selectlanguage{polish}š\selectlanguage{english}i\selectlanguage{polish}ć \selectlanguage{english}\& Ongena, 2020). The surfactin-induced activation of enhanced
immune responses in \emph{A. thaliana} is mediated by docking into
specific sphingolipid-enriched domains leading to host membrane
deformation and activation of mechanosensitive ion channels (Pr\selectlanguage{polish}š\selectlanguage{english}i\selectlanguage{polish}ć \selectlanguage{english}et
al., 2023).

Redox-mediated signalling

An intrinsic feature of both PAMP and MAMP triggered responses, as well
as physical and chemical perturbations to the plant plasma membrane, is
the propagation of waves of ROS and cytoplasmic calcium
({[}Ca\textsuperscript{2+}{]}\textsubscript{cyt}) accumulation from the
cell perceiving the signal to all cells throughout the plant (Fig. 2B).
Together with fluctuations in electric wave potentials, the ROS wave
triggers long-distance systemic defense signaling cascades that induce
IR throughout the plant. The ROS wave is an essential systemic signaling
system in plants, that contributes to plant-to-plant communication
(Szechy\selectlanguage{polish}ń\selectlanguage{english}ska-Hebda et al., 2022) and plant-to-microorganism interactions
(Y. Zhou et al., 2019). Moreover, this signaling system has now been
reported in a wide range of organisms (in microorganisms, plants, and
mammalian cells) and cell communities (Fichman, Rowland, Oliver, \&
Mittler, 2023). This universal cell-to-cell communication mechanism
probably evolved as part of the stress- or quorum-sensing mechanisms, is
a fundamental link between different organisms within a given
environment or ecosystem. The ``one health'' concept is based on
accumulating evidence that humans, animals, plants, microbiomes, and the
environment are inseparably interlinked and impact each other
constantly.

ROS signaling plays an important role in plant and animal interactions
with microorganisms. The ROS wave is triggered by the oxidative burst,
which occurs as a result of the activation of plasma membrane-bound
NADPH oxidases (Respiratory Burst Oxidase Homolgues: Rboh) and cell wall
peroxidases. These enzymes generate superoxide in the apoplastic space
i.e. the external space around the cell walls, which stores water and
nutrients. The oxidative burst is one of the earliest plant responses to
infection by microbes such as endophytes (Sahu et al., 2022). The
apoplast has a low antioxidant capacity but it is rich in antifreeze
proteins and pathogen-related proteins (PR-proteins) such as proteinase
inhibitors, defensins, thionins, and lipid transfer proteins that
together represent 23--33\% of the total apoplastic fluid proteins
(Farvardin et al., 2020).

In the case of pathogens, the prolonged activation of Rboh and other
ROS-producing enzymes results in the hypersensitive response (HR) that
prevents the spread of the pathogen from the attacked cell to
neighboring cells. Endophyte-triggered ROS generation does not lead to
HR but in contrast, triggers systemic signaling leading to defense gene
expression (Sahu et al., 2022) and wide-ranging enhanced protection
against biotic and abiotic stresses (Godara \& Ramakrishna, 2023). The
oxidative burst facilitates the oxidation of secondary compounds in the
apoplast/cell wall environment, such as the conversion of
sesquiterpenoids to oxygenous sesquiterpenoids through chemical
oxidation and differing degrees of oxidation. Endophytes also activate
the expression of genes encoding key enzymes involved in secondary
metabolism, such as those involved in sesquiterpenoid biosynthesis,
creating an array of sesquiterpenoid hydrocarbon scaffolds (J.-Y. Zhou,
Yuan, Li, Ning, \& Dai, 2016). For example, the microbe-induced
oxidative burst and oxygenous sesquiterpenoid accumulation occur
synchronously upon colonization of the medicinal
plant\emph{Atractylodeslancea} ~by~\emph{Pseudomonas fluorescens}
~ALEB7B. ~Sesquiterpenoids such as hinesol, \selectlanguage{greek}β-\selectlanguage{english}eudesmol, atractylone, and
caryophyllene oxide have medicinal properties protecting against
rheumatic diseases, digestive disorders, night blindness, and influenza
(J.-Y. Zhou et al., 2016).

Phytohormone-based signalling

Phytohormones such as SLs and karrikins (KARs) condition pre-symbiosis
rhizosphere communication with AMFs. \emph{Arabidopsis thaliana} (a
non-mycorrhizal plant) SLs and KARs receptors D14 (Dwarf14) and KAI2
(Karrikin-insensitive 2; rice homolog of D14L) activate downstream
signaling through the MAX2 (More axillary growth 2) E3 ligase. MAX2
targets different members of the SMAX1-LIKE (Suppressor of MAX2-1-like)
family of transcriptional repressors for degradation (Q. Wang, Smith, \&
Huang, 2022). The \emph{d14l} and \emph{d3} mutants show impaired AMF
colonization (Gutjahr et al., 2015). Perception of AMF by the rice
\selectlanguage{greek}α/β-\selectlanguage{english}fold hydrolase D14L (Dwarf14-Like; an evolutionary paralogue of D14)
leads to D3 (Dwarf3; a homolog of MAX2)-mediated signaling, stimulating
fungal metabolism, allowing rapid hyphal growth in roots and expanding
colonization. KAI2 functions are conserved in monocots (Meng et al.,
2022). SMAX1 operates downstream of the D14L/D3 receptor to negatively
regulate AMF symbiosis. Rice \emph{smax1} mutants show enhanced
expression of SL biosynthesis genes, indicating that SL-KAR crosstalk is
required for efficient AMF symbiosis (Choi et al., 2020).

Gibberellic acid (GA) and the associated GRAS family DELLA TFs mediate
transcriptional reprogramming during arbuscule development. GA binding
to its receptor induces the degradation of DELLA proteins that repress
GA signaling (Fig. 1A). The \emph{della} mutants of \emph{M.
truncatula}(Floss, Levesque-Tremblay, Park, \& Harrison, 2016) and rice
(Yu et al., 2014) exhibit impaired AMF symbiosis. Similarly, the
exogenous application of GA inhibited arbuscule branching in pea roots
(El Ghachtouli, Martin-Tanguy, Paynot, \& Gianinazzi, 1996). Expression
of the MIG1 (Mycorrhiza-induced GRAS1) GRAS-type TF, which is a key
regulator of cortical cell expansion, is a prerequisite for arbuscule
development. The expression of dominant-active DELLA proteins rescues
the loss-of-arbuscule phenotype of the \emph{mig1} mutants. Hence, MIG1
and DELLA act together to promote cortical radial cell expansion (Fig.
1A) (Heck et al., 2016). The MIG1-DELLA-mediated positive regulation
cascade is fine-tuned by MIG3 (a MIG1 paralogue)-SCL3 (Scarecrow-like 3,
GRAS TF), which acts as a negative regulator of arbuscule development
in\emph{M. truncatula} (Seemann et al., 2022). Salicylic acid (SA) also
regulates root/microbiome interactions in response to nutrient
deficiency (Kim et al., 2022). Rhizobia- and AMF-induced microbial
signals are transduced via nuclear-localized calcium oscillations,
generated by CNGC15 (Cyclic-nucleotide gated channel 15). The
calcium-bound form of calmodulin 2 (holo-CaM2) is required to sustain
prolonged CNGC15-dependent calcium oscillations. An engineered holo-CaM2
enhanced root nodule symbiosis but not arbuscular mycorrhization,
indicating that the holo-CaM2-CNGC15s module is specific to Rhizobial
symbiosis (Del Cerro et al., 2022). Calcium-phytohormone crosstalk
functions alongside bi-directional nutrient exchange to establish
rhizobia/AMF symbioses.

The light-induced GmSTF3/4 (soybean TGACG-motif binding factor 3/4) and
FLOWERING LOCUS T (GmFTs) proteins function as mobile shoot-to-root
signals. CCaMK (calcium- and calmodulin-dependent protein kinase)
mediated phosphorylation of GmSTF3 triggers the formation of a
GmSTF3--GmFT2a complex, which activates the expression of nodule
inception (NIN) and nuclear factor Y (NF-YA1 and NF-YB1) that together
regulate nodule organogenesis. The CCaMK--STF--FT module ensures a
sustained shoot carbon supply (T. Wang et al., 2021). Rhizobial
colonization, which is impaired in \emph{della} mutants, is tightly
controlled by host-derived GA signals. DELLA proteins promote the
formation of the CCaMK--IPD3 complex. They also interact with NSP2
(Nodulation Signaling Pathway2), enhancing the expression of
Nod-factor-inducible genes that are required for NSP1 binding to the NIN
promoter. In this way, DELLA integration of the IPD3 and NSP1/2 pathways
provides the transcriptional framework for successful root nodulation
(Jin et al., 2016).

While our knowledge of inter-organism ROS signal communication remains
rudimentary, it is evident that the cell-to-cell transmission of ROS
waves and its crosstalk with hormones is a central feature of
communication between the cells of a single organism and between
different organisms (Fichman, Zandalinas, Peck, Luan, \& Mittler, 2022).
For example, ROS-dependent auxin production in tomato shoots triggers
systemic signaling that enhances root strigolactone biosynthesis,
promoting AMF symbiosis, and thus increasing orthophosphate (Pi) uptake
and utilization (Zhou et al., 2019). Such studies provide new insights
into potential targets for the manipulation of symbiosis for high
nutrient utilization, particularly under future climate change
scenarios, where plant nutrient accumulation will be increasingly
challenged (Dong, Gruda, Lam, Li, \& Duan, 2018; Loladze, 2014).

Bi-directional nutrient exchange

The requirement for essential soil nutrients such as nitrogen (N) and
phosphate (P), is another major driver for symbiotic associations
between plants and beneficial microorganisms including AMFs and
nitrogen-fixing rhizobia. AMF establishes root symbiosis with more than
80\% of terrestrial plants (Chan, 2022; Dey \& Ghosh, 2022). The
partnership is mutually beneficial but not exclusive i.e. plants can
form associations with multiple microorganisms simultaneously. Such
associations assist plants in the acquisition of water and essential
minerals, particularly P and N (Wipf, Krajinski, van Tuinen, Recorbet,
\& Courty, 2019). In return, AMF and other microorganisms receive
assimilated carbon. AMF-mediated N/P uptake pathways function alongside
the plant nutrient transport systems, providing a greatly expanded
network of nutrient uptake from distal regions beyond the normal reach
of roots or root hairs.

Plants control the AMF symbioses to the availability of orthophosphate
(Pi), the preferred form of P taken up by roots (H. Lu et al., 2022).
The plant Pi sensing SYG1/Pho81/XPR1 (SPX)---PHOSPHATE STARVATION
RESPONSE (PHR) pathway regulates AMF symbiosis in crops such as rice
(Shi et al., 2021), \emph{Medicago} (J. Li et al., 2021) and tomato
(Liao et al., 2022). The SPXs Pi sensing proteins regulate the activity
of the PHR family of R2R3 MYB transcription factors (TF). Many genes
required for AMF symbiosis have PHR1-binding sites (P1BS) and are
activated by PHR binding (Fig. 1B). SPX negatively regulates PHR in rice
and tomato, and hence, suppresses AMF symbiosis under moderate-Pi or
Pi-replete conditions. In contrast, the \emph{Medicago} MtSPX1 and
MtSPX3 proteins are positive regulators of AMF colonization through the
regulation of strigolactone (SLs) biosynthesis. Thus, there appears to
be a diversification of SPX functions between cereals and legumes (J. Li
et al., 2021).

The activation of a subset of Pi-starvation induced or
phosphate-starvation response (PSR) genes, is a functional marker of
successful AMF symbiosis (Fig 1B). However, the genetic predisposition
of the host plant is a major determinant of the efficiency of AMF
symbiosis, as observed in maize accessions (Sawers et al., 2017). PHR2
(Phosphate Starvation Response 2) is a major transcription factor
regulating PSR in rice. It promotes AMF colonization by activating
pre-contact signaling genes and mediates mycorrhizal Pi uptake (Das et
al., 2022). The \emph{OsADK1} (Arbuscule Development Kinase 1)
receptor-like kinase, which is required for mycorrhizal colonization and
arbuscule development, is an OsPHR2 target (Shi et al., 2022).
The\emph{Rhizophagus irregularis} SPX-domain containing PTs regulates
arbuscule development and fine-tunes symbiotic Pi transfer -to the plant
(Xie et al., 2022). Similarly, the \emph{Gigaspora
margarita}high-affinity PT, GigmPT transceptor activates a protein
kinase A-mediated signaling cascade leading to Pi transport (Xie et al.,
2016). Other AMF-activated genes such as \emph{LjPT4} and \emph{MtPT4}
also serve Pi sensing functions in \emph{L. japonicus} and \emph{M.
truncatula} , respectively (Volpe, Giovannetti, Sun, Fiorilli, \&
Bonfante, 2016). The extraradical AMF also transports Pi-solubilizing
bacteria (PSB) that enhance organic P mineralization and increase Pi
delivery to plants, via AMF-independent pathways (F. Jiang, Zhang, Zhou,
George, \& Feng, 2021).

N availability regulates plant-AMF symbiosis through proteins such as
OsNPF4.5. Knockout lines lacking OsNPF4.5 functions had fewer arbuscules
and lower (45\%) symbiotic nitrate uptake (S. Wang et al., 2020). The
lipids and carbohydrates in root exudates support fungal growth (Kameoka
\& Gutjahr, 2022; Salmeron-Santiago et al., 2021). Lipid provision
involves two lipid biosynthetic enzymes (FatM and RAM2) and two ABC
transporters (STR1 and 2; Stunted Arbuscule 1 and 2). FatM (An acyl-ACP
thioesterase) increases plastid export of 16:0 fatty acids (Fig. 1A).
Thereafter, RAM2 (Required for Arbuscular Mycorrhization 2) produces
16:0 b-monoacylglycerol, which is exported from the root cells across
the peri-arbuscular membrane (Bravo, Brands, Wewer, Dormann, \&
Harrison, 2017). The \emph{M. truncatula} AP2/ERF family transcription
factor MtWRI5a binds to \emph{STR} and other AMF-specific gene promoters
(such as \emph{MtPT4} ) to promote lipid and Pi transport from
host-to-AMF and AMF-to-host, respectively (Y. Jiang et al., 2018). The
CBX1 (CTTC Motif-Binding Transcription Factor 1; a WRI1 homolog), which
is enriched in AMF-regulated genes, activates \emph{L. japonicus
LjPT4}and lipid-metabolism genes (Xue et al., 2018). The
rice\emph{Osadk1} -defective mutants have low expression of \emph{RAM1}
and\emph{WRI5} and produce fewer arbuscules (Shi et al., 2022). These
findings suggest that MtWRI5a, LjCBX1, and OsADK1 are master regulators
of bidirectional nutrient transport.

\textbf{PLANT HOLOBIONT ENHANCES ENVIRONMENTAL STRESS TOLERANCE}

Plant-associated microbial communities are known to impart tolerance
against salt (Chakraborty et al., 2021; H. Li et al., 2021) and drought
(Bazany et al., 2022; de Vries et al., 2020) stress conditions.
Salt-induced decreases in root nodulation (Singh \& Valdes-Lopez, 2023)
involve the expression of a glycogen synthase kinase 3 (GSK3)-like
kinase, GmSK2-8, which phosphorylates GmNSP1a, preventing the binding of
symbiotic genes such as \emph{GmNINa} and reducing nodulation (C. He et
al., 2021). The salt-inducible GmNAC181 TF activates
\emph{GmNINa}expression and maintains soybean nodulation under salt
stress (X. Wang et al., 2022). Drought triggers a compartment-specific
restructuring of rice root microbiota in rice, particularly in the
endosphere. Drought increases the prevalence of monoderm bacteria, which
lack an outer cell membrane and contain thick cell walls
(Santos-Medellin et al., 2021; Xu et al., 2018). Apart from providing
drought adaptation, the microbial communities also contribute to
drought-induced stress memory in rice, through compositional shifts that
help plants to survive better upon re-watering (Fig. 2B)
(Santos-Medellin et al., 2021). In the bioenergy model grass
\emph{Panicum hallii} , AMFs inoculation under water-limiting conditions
has been shown to impart resistance to sensitive bacterial communities
in the hydrosphere, indicating fungal-bacterial synergy (Hestrin et al.,
2022). However, these findings need more careful investigation, while
designing microbe-based solutions for realistic field scenarios. For
instance, drought-induced increased prevalence of beneficial microbes in
rhizosheaths has been demonstrated to induce risk factors for harmful
fungi (Lei, Ding, Xu, \& Zhang, 2023).

Stress as well as nutrient-limiting conditions have been shown to alter
innate immunity, which helps in recruiting beneficial microbes.
Pi-starvation induced transcriptional regulator PHR1 activates the
expression of \emph{RALF} (Rapid alkalinization factor) genes. RALF
peptides hijack the FERONIA kinase to suppress plant immunity and allow
colonization by specialized root microbiota such as \emph{Pseudomonas
fluorescens} (Fig. 2C) (Tang et al., 2022). FERONIA inhibitors,
including reversine and staurosporine, enhance innate immunity against
soil-borne diseases in tobacco, tomato, and rice without imposing growth
penalties (H. B. Liu et al., 2023). \emph{Feronia} mutants show low ROS
accumulation and harbor elevated levels of rhizosphere pseudomonads,
suggesting that FERONIA participates in the discrimination of beneficial
and harmful microbes (Song et al., 2021). Additionally, the
water-deficit conditions release flavonoids that reshape the root
microbiome by attracting \emph{Aeromonas} species that enhance
dehydration resistance in plants (D. He et al., 2022). Apart from plant
exudates, the core bacterial commensals and host tryptophan-derived
specialized metabolites also function to control the overgrowth of
fungal species (Wolinska et al., 2021), thereby maintaining host-microbe
as well as microbe-microbe homeostasis. Taken together, the role of
stress in shaping the plant microbial signature is clear; however, the
cause-effect relationship is yet to be established.

\textbf{BENEFICIAL PLANT-MICROBE INTERACTIONS: AN ECOLOGICAL
PERSPECTIVE}

The soil microbial community is intricately interwoven with plant
health. Beneficial plant-microbe interactions are an indispensable
component for restoring ecosystem loss due to excessive use of chemical
fertilizers and pesticides. For example, nitrogen (N) fertilizers are
responsible for nearly 5\% emissions of global greenhouse gas (GHG)
mainly nitrous oxide, which is 300 times more potent than
CO\textsubscript{2}, in terms of heat-trapping (Y. Gao \& Cabrera
Serrenho, 2023; Wen et al., 2021). Similarly, phosphorus (P) is another
rate-limiting nutrient and almost 80\% of applied P-fertilizer is lost
due to the inefficient acquisition by the plants, imposing an economic
burden on the farmers. The long-term excessive application of N- and
P-fertilizers causes soil acidification and eutrophication of
fresh-water bodies and is therefore not sustainable. Many beneficial
bacteria/fungi in the rhizosphere, collectively termed plant-growth
promoting microbes (PGPMs), support plant growth by increasing
nutrient-use efficiency, biotic/abiotic stress tolerance, and disease
resistance. Rhizobacteria and free-living diazotrophs mediate biological
N-fixation in nodulating and non-nodulating crops, respectively (Wen et
al., 2021). PGPMs also secrete different organic acids to solubilize
insoluble-P and hence, significantly reduce the usage of P-fertilizer,
without jeopardizing crop yield. Apart from fertilizers, the
over-application of chemical pesticides is another serious concern that
can increase resistance among pathogenic microbes. Besides, entering of
hazardous pesticides into the food chain can create a toxic ecosystem.
PGPMs serve as biological alternatives to these pesticides and hence,
maintain a disease-suppressive environment in soil, through multifaceted
ways including antibiosis, parasitism, competition for resources, and
predation in addition to providing induced systemic resistance in plants
(Fig. 4A). Along with mitigating biotic-stress, PGPMs also provide the
dual benefit of providing tolerance towards abiotic stresses, whose
occurrence increased as a repercussion of global climate change (Mitter,
Tosi, Obreg\selectlanguage{ngerman}ón, Dunfield, \& Germida, 2021). Intensive agricultural
practices also decrease the soil's organic carbon, deteriorating soil
fertility along with accelerating global warming as more carbon reaches
the environment. PGPMs use the photosynthesized CO\textsubscript{2}for
maintaining their growth and hence increase soil organic carbon,
contributing to climate restoration (Fig. 4A). Recently, a global scale
study has also established a positive correlation between
plant-mycorrhiza association and soil carbon content (Soudzilovskaia et
al., 2019). Climate change is also reshaping forest ecosystems by
driving species beyond their evolved resilience, with some of them even
facing the fate of extinction. Nurturing trees by microbial symbionts
acclimatized to specific climatic conditions safeguard their existence
by providing climate tolerance (Allsup, George, \& Lankau, 2023;
Baldrian, López-Mondéjar, \& Kohout, 2023). Taken together, supporting
the beneficial microbe-plant interactions will not only reduce the
negative impacts of climate change on plant fitness but, will also
reduce the use of chemical-based fertilizers/pesticides.

\textbf{BROADENING HOST-RANGE SPECIFICITY FOR PRODUCING ``GREENER''
CLIMATE}

The increasing levels of CO\textsubscript{2} in the atmosphere drive
photosynthesis and biomass accumulation in C3 crops (Ainsworth \& Long,
2021). This CO\textsubscript{2} fertilization effect increases plant
growth but negatively impacts crop nutritional quality (Myers et al.,
2014) with marked reductions in N, P, and other essential mineral
nutrients (McGrath \& Lobell, 2013). The increasing requirement for
essential soil nutrients is an important driver for improving symbiotic
associations between plants and beneficial microorganisms (Chan, 2022;
Dey \& Ghosh, 2022). Multiple approaches are underway to broaden
host-range specificity (Fig. 3) and to minimize high
CO\textsubscript{2}-induced decreases in crop quality. Of these,
altering and/or suppressing host-induced immunity is perhaps the most
important. For example, the downstream target of MtRAM1,
\emph{MtKIN3,}suppresses host defenses and supports AMF symbiosis
(Irving et al., 2022), while also regulating plant N responses. Rhizobia
produces several effectors that manipulate host defense signaling
pathways. For example, the soybean Nodulation outer protein T (NopT, an
effector protease from \emph{Sinorhizobium} sp.) activates the
GmPBS1-mediated resistance pathway and impairs nodule formation (Khan et
al., 2022). Similarly, the GmNNL1 (Nodule Number Locus 1; an R protein)
protein directly interacts with the NopP effector from
\emph{Bradyrhizobium}USDA110 to trigger immunity and inhibit nodulation
(B. Zhang et al., 2021). Thus, genetic engineering of effector proteins
to block defense but support symbiosis could broaden the range of
beneficial plant-microbe interaction (Fig. 3A). Dual-sensing receptors
can widen the host-range of beneficial microbes (Fig. 3B). For example,
the expression of chimeric ``Nod-Myc'' receptor in which the ectodomains
of OsMYR1 and OsCERK1 were replaced by homologous \emph{M. truncatula}
sequences in rice led to increased Nod factor-induced calcium
oscillations (J. He et al., 2019). Similarly, the binding affinity of
the \emph{L. Japonicas} receptor kinaseEPR3a (Exopolysaccharide receptor
3a) that binds AMF-specific glucans, as well as with rhizobia-specific
exopolysaccharide (EPS)could function as a dual receptor. In addition,
trans-kingdom signaling can also be exploited to enhance interactions
with beneficial microbes {[}85,86{]}. For example, barley lines
expressing the plant-derived signal rhizopine, which controls the
N\textsubscript{2}-fixation related gene expression in bacteria (Fig.
3C), can associate with\emph{Azorhizobium~caulinodans} , which has a
rhizopine uptake system and usually forms a nitrogen-fixing symbiosis
with \emph{Sesbania} .

For any PGPM, it is crucial to colonize as well as sustain in the
dynamic environment also called rhizo-competence which in part depends
on host genetics. Identification of intraspecific variation controlling
microbial selection and shaping root-associated microbiomes remains
challenging (Zboralski, Saadia, Novinscak, \& Filion, 2022).
Nevertheless, genome-wide association studies (GWAS) appear to be a
potentially powerful tool in identifying host genetic loci which are
microbes responsive (Fig. 3D). To explore this, previous efforts have
demonstrated, the dependence of rhizosphere microbial communities on
distinct genotypes of the same host species including maize and sorghum.
Moreover, in \emph{A. thaliana} host SNPs controlling defense and cell
wall integrity affected microbial community variation (Deng et al.,
2021). Such precision-based microbiome management in the future could
assist in engineering high-yielding/climate-resilient crops.

\textbf{ENGINEERING PLANT-MICROBE INTERACTION FOR NEXT GENERATION
AGRICULTURE}

The one health concept is based on a growing understanding that humans,
animals, plants, microbiomes, and the environment are inseparably linked
and impact each other constantly. The presence and stress levels
experienced by different organisms within an ecosystem could therefore
be transmitted from one to another through cell-to-cell ROS wave
signaling. Stress experiences may be transmitted between plants and the
soil microbiomes, by variations in the exchange of ROS signals. The
application of genetic engineering approaches that serve to support
symbiosis by blocking or minimizing the recognition-induced oxidative
burst and activating host defenses must take such interactions into
account, not only because they could increase the susceptibility of
plants to pathogen attack but because they could also disrupt or
interfere with a wide range of inter-organism communications within a
given ecosystem.

Next-generation agriculture will be comprised of at least three
components: enhanced crop production, minimal agri-inputs in the form of
pesticides/fertilizers, and enhanced microbial carbon sequestration
(Fig. 4A). Although, tailored plant-microbe interactions promise to meet
all these three expectations, the AKP (Anna Karenina Principle) must be
addressed. AKP considers that dysbiotic microbiomes are intrinsically
different, while healthy microbiota are similar (Arnault, Mony, \&
Vandenkoornhuyse, 2023). Nevertheless, some strategies have already
proved to be successful. For example, rhizosphere microbiome
transplantation (RMT), in which microbial communities from either
extreme environments or from a tolerant cultivar are inoculated to
enhance growth or suppress stress responses (Fig. 4B) (Poppeliers,
Sanchez-Gil, \& de Jonge, 2023). RMT-mediated enhanced plant growth is
poorly understood but could be stress-specific in nature. For example,
changes in the drought and cold tolerance of tree species were
associated with increased and decreased AMF diversity, respectively
(Allsup et al., 2023).

Manipulation of the soil microbiome, associated crop management
practices, and applied crop design are important components of solutions
to address climate change. Much attention has also focussed on
engineering nitrogen-fixing nodulation traits in non-leguminous crop
plants (Huisman \& Geurts, 2020). However, environmental perturbations
exert effects on the diversity of plant microbial communities, with
varying effects depending on the plant species and developmental stage.
For example, drought increases the release of flavonoids in root
exudates. These reshape the root microbiome by
attracting\emph{Aeromonas} species that enhance dehydration resistance
in plants (He et al., 2022). In addition, core bacterial commensals and
host tryptophan-derived specialized metabolites participate in the
control of fungal species (Wolinska et al., 2021). The changes in the
relative abundance of Actinobacteria and Proteobacteria were reported in
rice cultivated under drought conditions, an effect that persisted after
stress alleviation (Santos-Medellin et al., 2021). In sorghum, drought
increased the abundance of \emph{Actinobacteria} and decreased
pathogenic genera (\emph{Fusarium, Gibberella, and Sarocladium} )
compared with well-watered controls (Gao et al., 2020; Xu et al., 2018).
Drought-stressed sorghum plants in soils with
\emph{Arthrobacter}bacteria suffered more than those in which bacteria
of the genus\emph{Variovorax} were abundant (Qi et al., 2022). In
contrast,\emph{Arthrobacter} alleviated drought-stress effects in wheat
(Hone et al., 2021). The presence of endospheric \emph{Streptomyces} was
correlated with drought tolerance in several plant species (Fitzpatrick
et al., 2018).

Microbiome-inspired methods are promising innovations to enhance the
stress resilience of crops. Roots grown in natural- and agro-ecosystems
preferentially recruit PBB and AMF in drought situations (Song \& Haney,
2021; Williams \& de Vries, 2020; Zhao et al., 2023). Therefore,
commercial AMF inoculants, added as a supplement to agricultural lands,
have considerable potential in the alleviation of drought and nutrient
deficiency in plants (Salomon et al., 2022). The application of
microbial consortia may be more efficient than single-strain inocula in
enhancing stress tolerance (Bradá\selectlanguage{polish}č\selectlanguage{english}ov\selectlanguage{ngerman}á et al., 2019). However, while AMF
richness increases in barley roots under drought, AMF performance
(colonization and the abundance of arbuscules and vesicles) decreases,
indicating antagonistic interactions (Sendek et al., 2019). However,
while drought increases the prevalence of beneficial microbes in
rhizosheaths, it also increases the risk of penetration by harmful fungi
(Lei et al., 2023). Moreover, a limitation factor in the application of
such information concerns the diverse nature of AMF functionality
depending on environmental effects.

Native synthetic microbial communities (SynComs) from plants grown under
optimal conditions can be used to boost plant growth in poor soils (Fig.
4C) (M. Jiang et al., 2023). For example, SynComs application promotes
the growth of \emph{A. thaliana} , in an innate immunity-dependent
manner (Wolinska et al., 2021). Cross-kingdom (fungi and bacteria)
SynComs were more effective in suppressing fusarium-wilt disease in
tomato than fungi or bacteria alone (X. Zhou et al., 2022). RMT and
SynComs have yet to be tested for field applications, due to low
efficiency in isolating functionally beneficial microbiomes. Multiple
approaches based on screening natural variation, mathematical modeling,
RAMAN-spectra, and successive passaging are being used to map the
microbial community networks (Chen et al., 2021; X. He et al., 2021;
Morella et al., 2020). The root-secreted chemicals or exudates comprised
of photosynthetically fixed carbon as well as diverse signaling
molecules including \selectlanguage{greek}γ-\selectlanguage{english}aminobutyric acid, malate, and citrate, also
contribute to shaping rhizosphere microbiome (Fig. 4D) (W. Zhang \&
Mason, 2022).In addition, microbe-derived secretory proteins YukE cause
iron leakage in plant roots, which contributes to root colonization by
beneficial rhizobacterium \emph{Bacillus velezensis} (Y. Liu et al.,
2023). Microbiome engineering to improve the composition of root
exudates/secretomes will help determine the host-derived factors that
synchronize interactions between beneficial and resident microbiomes
(Escudero-Martinez \& Bulgarelli, 2023). QTLs that determine the
root-microbiota composition of crops contain genes such as the iron
regulator FIT and water channel aquaporin SlTIP2.3 in tomato (Oyserman
et al., 2022) and Nucleotide-Binding-Leucine-Rich-Repeat (NLR) in barley
(Escudero-Martinez et al., 2022). Apart from the genotypes, the
heritable component also needs to be accounted, especially in the
context of microbiome-assisted molecular crop breeding.

\textbf{CONCLUSION AND PERSPECTIVES}

In conclusion, recent advances confirm that the soil microbiome is key
to soil and plant health, as discussed above. It is perhaps not
surprising that plant-microbe interactions have not been exploited for
agricultural purposes ago, given the relatively poor indicators of
success under field conditions. However, our understanding of the
potential positive effects of PGPM has greatly increased in recent
years, as has our knowledge of underpinning mechanisms, particularly the
molecules involved in inter-organism communication. Thus, while there
are substantial gaps in current knowledge, plant-microbe interactions
are an attractive target for improving crop resilience and for achieving
sustainable yields under unfavourable environmental conditions.
Ultimately, the optimisation of plant-microbe interactions will be
pivotal to strategies aimed at the long-term carbon sequestration in
soils that is crucial to nature-based solutions to climate change.
Microorganisms are at the core of the global carbon cycle, not least
because they are responsible for more than 50\% of annual
CO\textsubscript{2/}methane transformations and contribute to almost
50\% of the annual global CO\textsubscript{2}-sequestration. Engineering
a more sustainable carbon cycle requires a detailed molecular
mechanism-based understanding of the enzymes involved in
CO\textsubscript{2}/methane interconversions. This essential knowledge
is a prerequisite for viable microbe-based solutions to climate change.

Tailoring the soil microbiome to boost plant yield is currently
restricted to agricultural practices and adding probiotic microbial
consortia, largely because gene editing approaches are limited by
societal acceptance. Ambitious objectives have been set in Europe and in
other continents to ensure food sovereignty, while enhancing
agricultural sustainability. Such targets have to incorporate climate
change reliance traits, together with a much higher efficiency in the
use of essential resources particularly water, and soil nutrients. An
ultimate aim is to reduce reliance on fertilizers and plant protection
products. It will not be possible to achieve these goals without a
revolution in plant breeding that includes a continuous flow of
innovation and technology transfer, incorporating new knowledge as it
becomes available. This requires a substantial acceleration in the
development of new plant varieties that have improved microbial
associations, and so can use available resources much more efficiently,
and are better adapted to climate change. The rapid introduction of such
varieties will only be possible if breeders have access to all of the
available tools and technologies, and crucially that Government
registration and legislation accepts new genomic technologies that are
at the heart of current accelerated breeding opportunities.

Nano-enabled approaches have the potential to overcome the limitations
of traditional microbiome engineering, such as the absence of
specificity in attaining targeted manipulation, collateral fatality to
microbial diversity, and lack of reliable robust results (Fig. 4E)
(Hussain et al., 2023; You, Kerner, Shanmugam, \& Khodakovskaya, 2023).
However, the application of novel nanomaterials still requires
comprehensive profiling to evaluate long-term efficacy on plant
productivity and ecosystem health (Ahmed, Noman, Gardea-Torresdey,
White, \& Li, 2023). To date, the beneficial actions of such approaches
have been studied largely under controlled conditions and hence
effective translation into the field is uncertain. The practical
relevance of increasing mechanistic knowledge hence requires extensive
study under field conditions, where environmental constraints influence
to composition and effectiveness of plant/microbiome interactions. Such
information is essential to understand how we might best apply
inoculants to fields, which remains a significant challenge (Kaminsky et
al. 2018). Nevertheless, the strategies discussed above have as yet
untapped potential, and are particularly important in developing
countries (Ashwathi, 2019).

Soil microbial communities are not constant and vary according to
developmental stage, tissue type, and sampling time (Quiza et al.,
2023). Our increasing knowledge of the leaf and root microbiomes has
demonstrated the diversity of bacteria that are adapted for survival on,
as well as within plants. The phyllosphere is a conducive niche for
horizontal gene transfer (HGT)~between epiphytic bacterial strains,~the
plant surface thus provides a niche for the evolution of new variants.
Gaining a deeper understanding of this dynamic environment for gene
exchange and the emergence of new strains, together with the
exploitation of the remarkable genomic diversity within epiphytic
populations, will help overcome current limitations in host-range
specificity and allow potential jumping to other host plants. This
together, with a better understanding of the plethora of signalling
molecules including ROS (and associated redox post-translational
modifications) that contribute to the dialogue between plants and
microbes, will provide an improved road map for exploitation of the
bi/tri/multi-partite interactions with beneficial microbes that will
underpin sustainable next-generation agriculture.

\textbf{ACKNOWLEDGMENT}

CHF thanks the Science and Engineering Research Board of India for a
VAJRA fellowship (VJR/2019/000068).

\emph{}

\textbf{REFERENCES}

Ahmed, T., Noman, M., Gardea-Torresdey, J. L., White, J. C., \& Li, B.
(2023). Dynamic interplay between nano-enabled agrochemicals and the
plant-associated microbiome. \emph{Trends in Plant Science, 28} (11),
1310-1325.

Ainsworth, E. A., \& Long, S. P. (2021). 30 years of free-air carbon
dioxide enrichment (FACE): What have we learned about future crop
productivity and its potential for adaptation? \emph{Global Change
Biology, 27} (1), 27-49.

Allsup, C. M., George, I., \& Lankau, R. A. (2023). Shifting microbial
communities can enhance tree tolerance to changing
climates.\emph{Science, 380} , 835-840.

Andri\selectlanguage{polish}ć, \selectlanguage{english}S., Meyer, T., Rigolet, A., Prigent-Combaret, C., H\selectlanguage{ngerman}öfte, M.,
Balleux, G., . . . McCann, A. (2021). Lipopeptide interplay mediates
molecular interactions between soil Bacilli and
Pseudomonads.\emph{Microbiology Spectrum, 9} , e02038-02021.

Arnault, G., Mony, C., \& Vandenkoornhuyse, P. (2023). Plant microbiota
dysbiosis and the Anna Karenina Principle. \emph{Trends Plant Science,
28} , 18-30.

Awasthi, A. Field-specific microbial consortia are feasible: A response
to Kaminsky et al. (2019). \emph{Trends in Biotechnology, 37} , 569-572.

Bai, B., Liu, W., Qiu, X., Zhang, J., Zhang, J., \& Bai, Y. (2022). The
root microbiome: Community assembly and its contributions to plant
fitness. \emph{Journal of Integrative Plant Biology, 64} , 230-243.

Baldrian, P., López-Mondéjar, R., \& Kohout, P. (2023). Forest
microbiome and global change. \emph{Nature Reviews Microbiology}
,\emph{21} , 487--501.

Banerjee, S., \& van der Heijden, M. G. (2023). Soil microbiomes and one
health. \emph{Nature Reviews Microbiology, 21} , 6-20.

Bazany, K. E., Wang, J. T., Delgado-Baquerizo, M., Singh, B. K., \&
Trivedi, P. (2022). Water deficit affects inter-kingdom microbial
connections in plant rhizosphere. \emph{Environmental Microbiology 24}
(8), 3722-3734.

Bradá\selectlanguage{polish}č\selectlanguage{english}ov\selectlanguage{ngerman}á, K., Florea, A. S., Bar-Tal, A., Minz, D., Yermiyahu, U.,
Shawahna, R., . . . Dietel, K. (2019). Microbial consortia versus
single-strain inoculants: an advantage in PGPM-assisted tomato
production? \emph{Agronomy, 9} (2), 105.

Bravo, A., Brands, M., Wewer, V., Dormann, P., \& Harrison, M. J.
(2017). Arbuscular mycorrhiza-specific enzymes FatM and RAM2 fine-tune
lipid biosynthesis to promote development of arbuscular
mycorrhiza.\emph{New Phytologist, 214} (4), 1631-1645.
doi:10.1111/nph.14533

Cawoy, H., Debois, D., Franzil, L., De Pauw, E., Thonart, P., \& Ongena,
M. (2015). Lipopeptides as main ingredients for inhibition of fungal
phytopathogens by \emph{Bacillus subtilis} /\emph{amyloliquefaciens}
.\emph{Microbial Biotechnology, 8} (2), 281-295.

Chakraborty, S., Driscoll, H. E., Abrahante, J. E., Zhang, F., Fisher,
R. F., \& Harris, J. M. (2021). Salt stress enhances early symbiotic
gene expression in \emph{Medicago truncatula} and induces a
stress-specific set of \emph{Rhizobium} -responsive
genes.\emph{Molecular Plant Microbe Interactions, 34} (8), 904-921.

Chan, C. (2022). Establishing AM symbiosis: Letting friends stay only
when you need their gifts. In: Oxford University Press.

Chen, Q. L., Hu, H. W., He, Z. Y., Cui, L., Zhu, Y. G., \& He, J. Z.
(2021). Potential of indigenous crop microbiomes for sustainable
agriculture. \emph{Nature Food, 2} (4), 233-240.

Choi, J., Lee, T., Cho, J., Servante, E. K., Pucker, B., Summers, W., .
. . Paszkowski, U. (2020). The negative regulator SMAX1 controls
mycorrhizal symbiosis and strigolactone biosynthesis in
rice.\emph{Nature Communications, 11} (1), 2114.

Das, D., Paries, M., Hobecker, K., Gigl, M., Dawid, C., Lam, H.-M., . .
. Gutjahr, C. (2022). PHOSPHATE STARVATION RESPONSE transcription
factors enable arbuscular mycorrhiza symbiosis. \emph{Nature
Communications, 13} (1), 1-12.

de Vries, F. T., Griffiths, R. I., Knight, C. G., Nicolitch, O., \&
Williams, A. (2020). Harnessing rhizosphere microbiomes for
drought-resilient crop production. \emph{Science, 368} (6488), 270-274.

Del Cerro, P., Cook, N. M., Huisman, R., Dangeville, P., Grubb, L. E.,
Marchal, C., . . . Charpentier, M. (2022). Engineered CaM2 modulates
nuclear calcium oscillation and enhances legume root nodule
symbiosis.\emph{Proceedings of the National Academy of Sciences USA,
119} (13), e2200099119.

Deng, S., Caddell, D. F., Xu, G., Dahlen, L., Washington, L., Yang, J.,
\& Coleman-Derr, D. (2021). Genome wide association study reveals plant
loci controlling heritability of the rhizosphere microbiome. \emph{The
ISME Journal, 15} (11), 3181-3194.

Dey, M., \& Ghosh, S. (2022). Arbuscular mycorrhizae in plant immunity
and crop pathogen control. \emph{Rhizosphere} , 100524.

Dong, J., Gruda, N., Lam, S. K., Li, X., \& Duan, Z. (2018). Effects of
elevated CO2 on nutritional quality of vegetables: a
review.\emph{Frontiers in Plant Science, 9} , 924.

El Ghachtouli, N., Martin-Tanguy, J., Paynot, M., \& Gianinazzi, S.
(1996). First report of the inhibition of arbuscular mycorrhizal
infection of \emph{Pisum sativum} by specific and irreversible
inhibition of polyamine biosynthesis or by gibberellic acid
treatment.\emph{FEBS Letters, 385} (3), 189-192.

Escudero-Martinez, C., \& Bulgarelli, D. (2023). Engineering the crop
microbiota through host genetics. \emph{Annual Review of Phytopathology,
61} , 257-277.

Escudero-Martinez, C., Coulter, M., Alegria Terrazas, R., Foito, A.,
Kapadia, R., Pietrangelo, L., . . . Morris, J. (2022). Identifying plant
genes shaping microbiota composition in the barley
rhizosphere.\emph{Nature Communications, 13} (1), 3443.

Farvardin, A., González-Hernández, A., Llorens, E., García-Agustín, P.,
Scalschi, L., \& Vicedo, B. (2020). The apoplast: a key player in plant
survival. \emph{Antioxidants} (Basel) \emph{9} (7): 604. In.

Fichman, Y., Rowland, L., Oliver, M. J., \& Mittler, R. (2023). ROS are
evolutionary conserved cell-to-cell stress signals. \emph{Proceedings of
the National Academy of Sciences USA 120} (31), e2305496120.

Fichman, Y., Zandalinas, S. I., Peck, S., Luan, S., \& Mittler, R.
(2022). HPCA1 is required for systemic reactive oxygen species and
calcium cell-to-cell signaling and plant acclimation to stress.\emph{The
Plant Cell, 34} (11), 4453-4471.

Fitzpatrick, C. R., Copeland, J., Wang, P. W., Guttman, D. S., Kotanen,
P. M., \& Johnson, M. T. (2018). Assembly and ecological function of the
root microbiome across angiosperm plant species. \emph{Proceedings of
the National Academy of Sciences, 115} (6), E1157-E1165.

Floss, D. S., Levesque-Tremblay, V., Park, H. J., \& Harrison, M. J.
(2016). DELLA proteins regulate expression of a subset of AM
symbiosis-induced genes in \emph{Medicago truncatula} . \emph{Plant
Signaling Behaviour, 11} (4), e1162369.

Gao, C., Montoya, L., Xu, L., Madera, M., Hollingsworth, J., Purdom, E.,
. . . Dahlberg, J. A. (2020). Fungal community assembly in
drought-stressed sorghum shows stochasticity, selection, and universal
ecological dynamics. \emph{Nature Communications, 11} (1), 34.

Gao, Y., \& Cabrera Serrenho, A. (2023). Greenhouse gas emissions from
nitrogen fertilizers could be reduced by up to one-fifth of current
levels by 2050 with combined interventions. \emph{Nature Food, 4} (2),
170-178.

Ghatak, A., Chaturvedi, P., Waldherr, S., Subbarao, G. V., \& Weckwerth,
W. (2023). PANOMICS at the interface of root-soil microbiome and
BNI.\emph{Trends in Plant Science, 28} (1), 106-122.

Godara, H., \& Ramakrishna, W. (2023). Endophytes as nature's gift to
plants to combat abiotic stresses. \emph{Letters in Applied
Microbiology, 76} (2), ovac067.

Gutjahr, C., Gobbato, E., Choi, J., Riemann, M., Johnston, M. G.,
Summers, W., . . . Paszkowski, U. (2015). Rice perception of symbiotic
arbuscular mycorrhizal fungi requires the karrikin receptor
complex.\emph{Science, 350} (6267), 1521-1524.

Gysel, K., Laursen, M., Thygesen, M. B., Lironi, D., Bozsoki, Z.,
Hjuler, C. T., . . . Andersen, K. R. (2021). Kinetic proofreading of
lipochitooligosaccharides determines signal activation of symbiotic
plant receptors. \emph{Proceedings of the National Academy of Sciences
USA, 118} (44).

He, C., Gao, H., Wang, H., Guo, Y., He, M., Peng, Y., \& Wang, X.
(2021). GSK3-mediated stress signaling inhibits legume-rhizobium
symbiosis by phosphorylating GmNSP1 in soybean. \emph{Molecuar Plant,
14} (3), 488-502.

He, D., Singh, S. K., Peng, L., Kaushal, R., Vilchez, J. I., Shao, C., .
. . Zhang, H. (2022). Flavonoid-attracted Aeromonas sp. from the
Arabidopsis root microbiome enhances plant dehydration
resistance.\emph{The ISME Journal, 16} (11), 2622-2632.

He, J., Zhang, C., Dai, H., Liu, H., Zhang, X., Yang, J., . . . Wang, E.
(2019). A LysM Receptor Heteromer Mediates Perception of Arbuscular
Mycorrhizal Symbiotic Signal in Rice. \emph{Molecular Plant, 12} (12),
1561-1576.

He, X., Zhang, Q., Li, B., Jin, Y., Jiang, L., \& Wu, R. (2021). Network
mapping of root--microbe interactions in Arabidopsis thaliana. \emph{npj
Biofilms and Microbiomes, 7} (1), 72.

Heck, C., Kuhn, H., Heidt, S., Walter, S., Rieger, N., \& Requena, N.
(2016). Symbiotic fungi control plant root cortex development through
the novel GRAS transcription factor MIG1. \emph{Current Biology, 26}
(20), 2770-2778.

Hestrin, R., Kan, M., Lafler, M., Wollard, J., Kimbrel, J. A., Ray, P.,
. . . Pett-Ridge, J. (2022). Plant-associated fungi support bacterial
resilience following water limitation. \emph{The ISME Journal, 16} (12),
2752-2762.

Hoff, G., Arguelles Arias, A., Boubsi, F., Pr\selectlanguage{polish}š\selectlanguage{english}i\selectlanguage{polish}ć, \selectlanguage{english}J., Meyer, T.,
Ibrahim, H. M., . . . Franzil, L. (2021). Surfactin stimulated by pectin
molecular patterns and root exudates acts as a key driver of the
Bacillus-plant mutualistic interaction. \emph{MBio, 12} (6),
e01774-01721.

Hone, H., Mann, R., Yang, G., Kaur, J., Tannenbaum, I., Li, T., . . .
Sawbridge, T. (2021). Profiling, isolation and characterisation of
beneficial microbes from the seed microbiomes of drought tolerant
wheat.\emph{Scientific Reports, 11} (1), 11916.

Huisman, R., \& Geurts, R. (2020). A roadmap toward engineered
nitrogen-fixing nodule symbiosis. \emph{Plant Communications, 1} (1).

Hussain, M., Zahra, N., Lang, T., Zain, M., Raza, M., Shakoor, N., . . .
Zhou, H. (2023). Integrating nanotechnology with plant microbiome for
next-generation crop health. \emph{Plant Physiology and Biochemistry,
196} , 703-711.

Irving, T. B., Chakraborty, S., Ivanov, S., Schultze, M., Mysore, K. S.,
Harrison, M. J., \& Ane, J. M. (2022). KIN3 impacts arbuscular
mycorrhizal symbiosis and promotes fungal colonisation in \emph{Medicago
truncatula} . \emph{The Plant Journal, 110} (2), 513-528.

Jiang, F., Zhang, L., Zhou, J., George, T. S., \& Feng, G. (2021).
Arbuscular mycorrhizal fungi enhance mineralisation of organic
phosphorus by carrying bacteria along their extraradical
hyphae.\emph{New Phytologist, 230} (1), 304-315.

Jiang, M., Delgado-Baquerizo, M., Yuan, M. M., Ding, J., Yergeau, E.,
Zhou, J., . . . Liang, Y. (2023). Home-based microbial solution to boost
crop growth in low-fertility soil. \emph{New Phytologist, 239,} 752-765.

Jiang, Y., Xie, Q., Wang, W., Yang, J., Zhang, X., Yu, N., . . . Wang,
E. (2018). Medicago AP2-Domain Transcription Factor WRI5a Is a Master
Regulator of Lipid Biosynthesis and Transfer during Mycorrhizal
Symbiosis. \emph{Molecular Plant, 11} , 1344-1359.

Jin, Y., Liu, H., Luo, D., Yu, N., Dong, W., Wang, C., . . . Wang, E.
(2016). DELLA proteins are common components of symbiotic rhizobial and
mycorrhizal signalling pathways. \emph{Nature Communications, 7} ,
12433.

Kameoka, H., \& Gutjahr, C. (2022). Functions of lipids in development
and reproduction of arbuscular mycorrhizal fungi. \emph{Plant Cell
Physiology, 63} , 1356-1365.

Kaminsky,~L.M., Trexler, R., Malik, R.J., Hockett, K.L., Bell, T.H.
(2019) The inherent conflicts in developing soil microbial
inoculants\emph{Trends in Biotechnology,~37} , 140-151.

Ke, J., Wang, B., Yoshikuni, Y., (2021) Microbiome engineering:
Synthetic biology of plant-associated microbiomes in sustainable
agriculture. \emph{Trends in Biotechnology, 39} , 244-261.

Kelly, S., Radutoiu, S., \& Stougaard, J. (2017). Legume LysM receptors
mediate symbiotic and pathogenic signalling. \emph{Current Opinion in
Plant Biology, 39} , 152-158.

Khan, A., Wadood, S. F., Chen, M., Wang, Y., Xie, Z. P., \& Staehelin,
C. (2022). Effector-triggered inhibition of nodulation: A rhizobial
effector protease targets soybean kinase GmPBS1-1. \emph{Plant
Physiology 189} , 2382-2395.

Kim, B., Westerhuis, J. A., Smilde, A. K., Flokova, K., Suleiman, A. K.
A., Kuramae, E. E., . . . Zancarini, A. (2022). Effect of strigolactones
on recruitment of the rice root-associated microbiome. \emph{FEMS
Microbiological Ecology, 98} .

Lei, Z., Ding, Y., Xu, W., \& Zhang, Y. (2023). Microbial Community
Structure in rice rhizosheaths under drought stress. \emph{Journal of
Plant Ecology, 16} (5), rtad012.

Li, H., La, S., Zhang, X., Gao, L., \& Tian, Y. (2021). Salt-induced
recruitment of specific root-associated bacterial consortium capable of
enhancing plant adaptability to salt stress. \emph{The ISME Journal, 15}
, 2865-2882.

Li, J., Yuan, D., Wang, P., Wang, Q., Sun, M., Liu, Z., . . . Zhang, B.
(2021). Cotton pan-genome retrieves the lost sequences and genes during
domestication and selection. \emph{Genome Biology, 22} , 1-26.

Liao, D., Sun, C., Liang, H., Wang, Y., Bian, X., Dong, C., . . . Chen,
A. (2022). SlSPX1-SlPHR complexes mediate the suppression of arbuscular
mycorrhizal symbiosis by phosphate repletion in tomato. \emph{The Plant
Cell, 34} , 4045-4065.

Liu, H. B., Li, X., Cai, J., Jiang, L. L., Zhang, X., Wu, D., . . . Yu,
F. (2023). A screening of inhibitors targeting the receptor kinase
FERONIA reveals small molecules that enhance plant root
immunity.\emph{Plant Biotechnology Journal 21} , 63-77.

Liu, J., Wang, T., Qin, Q., Yu, X., Yang, S., Dinkins, R. D., . . . Zhu,
H. (2022). Paired Medicago receptors mediate broad-spectrum resistance
to nodulation by Sinorhizobium meliloti carrying a species-specific
gene. \emph{Proceedings of the National Academy of Sciences of the USA,
119} , e2214703119.

Liu, Y., Shu, X., Chen, L., Zhang, H., Feng, H., Sun, X., . . . Xu, Z.
(2023). Plant commensal type VII secretion system causes iron leakage
from roots to promote colonization. \emph{Nature Microbiology} , 1-16.

Loladze, I. (2014). Hidden shift of the ionome of plants exposed to
elevated CO2 depletes minerals at the base of human
nutrition.\emph{elife, 3} , e02245.

Lu, H., Wang, F., Wang, Y., Lin, R., Wang, Z., \& Mao, C. (2022).
Molecular mechanisms and genetic improvement of low-phosphorus tolerance
in rice. \emph{Plant Cell \& Environment, 46,} 1104-1119.

Lu, P., Liu, Y., Yu, X., Shi, C. L., \& Liu, X. (2022). The right
microbe-associated molecular patterns for effective recognition by
plants. \emph{Frontiers in Microbiology, 13} , 1019069.

McGrath, J. M., \& Lobell, D. B. (2013). Reduction of transpiration and
altered nutrient allocation contribute to nutrient decline of crops
grown in elevated CO(2) concentrations. \emph{Plant Cell \& Environment,
36} (3), 697-705.

Meng, Y., Varshney, K., Incze, N., Badics, E., Kamran, M., Davies, S.
F., . . . Waters, M. T. (2022). KARRIKIN INSENSITIVE2 regulates leaf
development, root system architecture and arbuscular-mycorrhizal
symbiosis in \emph{Brachypodium distachyon} . \emph{The Plant Journal,
109} (6), 1559-1574.

Mitter, E. K., Tosi, M., Obreg\selectlanguage{ngerman}ón, D., Dunfield, K. E., \& Germida, J. J.
(2021). Rethinking crop nutrition in times of modern microbiology:
innovative biofertilizer technologies. \emph{Frontiers in Sustainable
Food Systems, 5} , 606815.

Morella, N. M., Weng, F. C., Joubert, P. M., Metcalf, C. J. E., Lindow,
S., \& Koskella, B. (2020). Successive passaging of a plant-associated
microbiome reveals robust habitat and host genotype-dependent
selection.\emph{Proceedings of the National Academy of Sciences USA,
117} (2), 1148-1159.

Myers, S. S., Zanobetti, A., Kloog, I., Huybers, P., Leakey, A. D.,
Bloom, A. J., . . . Usui, Y. (2014). Increasing CO2 threatens human
nutrition. \emph{Nature, 510} (7503), 139-142.

Nelson, E. B. (2018). The seed microbiome: origins, interactions, and
impacts. \emph{Plant and Soil, 422} , 7-34.

Nelson, E. B., Simoneau, P., Barret, M., Mitter, B., \& Compant, S.
(2018). Editorial special issue: the soil, the seed, the microbes and
the plant. In (Vol. 422, pp. 1-5): Springer.

Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., . .
. Thonart, P. (2007). Surfactin and fengycin lipopeptides of Bacillus
subtilis as elicitors of induced systemic resistance in
plants.\emph{Environmental Microbiology, 9} (4), 1084-1090.

Oyserman, B. O., Flores, S. S., Griffioen, T., Pan, X., van der Wijk,
E., Pronk, L., . . . Movassagh, M. (2022). Disentangling the genetic
basis of rhizosphere microbiome assembly in tomato. \emph{Nature
Communications, 13} (1), 3228.

Poppeliers, S. W., Sanchez-Gil, J. J., \& de Jonge, R. (2023). Microbes
to support plant health: understanding bioinoculant success in complex
conditions. \emph{Current Opinion in Microbiology, 73} , 102286.

Pr\selectlanguage{polish}š\selectlanguage{english}i\selectlanguage{polish}ć, \selectlanguage{english}J., Gilliard, G., Ibrahim, H., Arg\selectlanguage{ngerman}üelles-Arias, A., Rondelli, V.,
Crowet, J.-M., . . . Nasir, M. N. (2023). Mechanosensing and
Sphingolipid-Docking Mediate Lipopeptide-Induced Immunity in
Arabidopsis. \emph{bioRxiv} , 2023.2007. 2004.547613.

Pr\selectlanguage{polish}š\selectlanguage{english}i\selectlanguage{polish}ć, \selectlanguage{english}J., \& Ongena, M. (2020). Elicitors of plant immunity triggered
by beneficial bacteria. \emph{Frontiers in Plant Science, 11} , 594530.

Qi, M., Berry, J. C., Veley, K. M., O'Connor, L., Finkel, O. M.,
Salas-Gonz\selectlanguage{ngerman}ález, I., . . . Glavina del Rio, T. (2022). Identification of
beneficial and detrimental bacteria impacting sorghum responses to
drought using multi-scale and multi-system microbiome
comparisons.\emph{The ISME journal, 16} (8), 1957-1969.

Quiza, L., Tremblay, J., Pagé, A. P., Greer, C. W., Pozniak, C. J., Li,
R., . . . Yergeau, E. (2023). The effect of wheat genotype on the
microbiome is more evident in roots and varies through time. \emph{ISME
Communications, 3} , 32.

Saad, M.M., Eida, A.A., Hirt, H. (2020) Tailoring plant-associated
microbial inoculants in agriculture: a roadmap for successful
application,~\emph{Journal of Experimental Botany} , \emph{71} ,
3878--3901,

Sahu, P. K., Jayalakshmi, K., Tilgam, J., Gupta, A., Nagaraju, Y.,
Kumar, A., . . . Rajput, V. D. (2022). ROS generated from biotic stress:
Effects on plants and alleviation by endophytic microbes.\emph{Frontiers
in Plant Science, 13} , 1042936.

Salmeron-Santiago, I. A., Martinez-Trujillo, M., Valdez-Alarcon, J. J.,
Pedraza-Santos, M. E., Santoyo, G., Pozo, M. J., \& Chavez-Barcenas, A.
T. (2021). An Updated Review on the Modulation of Carbon Partitioning
and Allocation in Arbuscular Mycorrhizal Plants. \emph{Microorganisms,
10} (1).

Salomon, M., Demarmels, R., Watts-Williams, S., McLaughlin, M., Kafle,
A., Ketelsen, C., . . . van der Heijden, M. G. (2022). Global evaluation
of commercial arbuscular mycorrhizal inoculants under greenhouse and
field conditions. \emph{Applied Soil Ecology, 169} , 104225.

Santos-Medellin, C., Liechty, Z., Edwards, J., Nguyen, B., Huang, B.,
Weimer, B. C., \& Sundaresan, V. (2021). Prolonged drought imparts
lasting compositional changes to the rice root microbiome. \emph{Nature
Plants, 7} (8), 1065-1077.

Sawers, R. J., Svane, S. F., Quan, C., Gronlund, M., Wozniak, B.,
Gebreselassie, M. N., . . . Paszkowski, U. (2017). Phosphorus
acquisition efficiency in arbuscular mycorrhizal maize is correlated
with the abundance of root-external hyphae and the accumulation of
transcripts encoding PHT1 phosphate transporters. \emph{New Phytologist,
214} (2), 632-643.

Seemann, C., Heck, C., Voß, S., Schmoll, J., Enderle, E., Schwarz, D.,
\& Requena, N. (2022). Root cortex development is fine\selectlanguage{english}-tuned by the
interplay of MIGs, SCL3 and DELLAs during arbuscular mycorrhizal
symbiosis. \emph{New Phytologist, 233} (2), 948-965.

Sendek, A., Karakoc, C., Wagg, C., Dominguez-Begines, J., do Couto, G.
M., van der Heijden, M. G., . . . Klotz, S. (2019). Drought modulates
interactions between arbuscular mycorrhizal fungal diversity and barley
genotype diversity. \emph{Scientific reports, 9} (1), 9650.

Shi, J., Zhao, B., Jin, R., Hou, L., Zhang, X., Dai, H., . . . Wang, E.
(2022). A phosphate starvation response-regulated receptor-like kinase,
OsADK1, is required for mycorrhizal symbiosis and phosphate starvation
responses. \emph{New Phytologist, 236} (6), 2282-2293.

Shi, J., Zhao, B., Zheng, S., Zhang, X., Wang, X., Dong, W., . . . Wang,
E. (2021). A phosphate starvation response-centered network regulates
mycorrhizal symbiosis. \emph{Cell, 184} (22), 5527-5540 e5518.

Singh, J., \& Valdes-Lopez, O. (2023). Discovering the genetic modules
controlling root nodule symbiosis under abiotic stresses: salinity as a
case study. \emph{New Phytologist, 237} (4), 1082-1085.

Sohrabi, R., Paasch, B. C., Liber, J. A., \& He, S. Y. (2023).
Phyllosphere Microbiome. \emph{Annual Review of Plant Biology 74} ,
539-568.

Song, Y., \& Haney, C. H. (2021). Drought dampens microbiome
development. \emph{Nature Plants, 7} (8), 994-995.

Song, Y., Wilson, A. J., Zhang, X.-C., Thoms, D., Sohrabi, R., Song, S.,
. . . He, S. Y. (2021). FERONIA restricts Pseudomonas in the rhizosphere
microbiome via regulation of reactive oxygen species. \emph{Nature
plants, 7} (5), 644-654.

Soudzilovskaia, N. A., van Bodegom, P. M., Terrer, C., Zelfde, M. v. t.,
McCallum, I., Luke McCormack, M., . . . Tedersoo, L. (2019). Global
mycorrhizal plant distribution linked to terrestrial carbon
stocks.\emph{Nature Communications, 10} (1), 5077.

Szechy\selectlanguage{polish}ń\selectlanguage{english}ska-Hebda, M., Lewandowska, M., Wito\selectlanguage{polish}ń, \selectlanguage{english}D., Fichman, Y., Mittler,
R., \& Karpi\selectlanguage{polish}ń\selectlanguage{english}ski, S. M. (2022). Aboveground plant-to-plant electrical
signaling mediates network acquired acclimation. \emph{The Plant Cell,
34} (8), 3047-3065.

Tang, J., Wu, D., Li, X., Wang, L., Xu, L., Zhang, Y., . . . Dai, S.
(2022). Plant immunity suppression via PHR1-RALF-FERONIA shapes the root
microbiome to alleviate phosphate starvation. \emph{The EMBO Journal,
41} (6), e109102.

Trivedi, P., Batista, B. D., Bazany, K. E., \& Singh, B. K. (2022).
Plant--microbiome interactions under a changing world: Responses,
consequences and perspectives. \emph{New Phytologist, 234} (6),
1951-1959.

Turner, T. R., James, E. K., \& Poole, P. S. (2013). The plant
microbiome. \emph{Genome Biology, 14} (6), 209.

Volpe, V., Giovannetti, M., Sun, X. G., Fiorilli, V., \& Bonfante, P.
(2016). The phosphate transporters LjPT4 and MtPT4 mediate early root
responses to phosphate status in non mycorrhizal roots. \emph{Plant Cell
\& Environment, 39} (3), 660-671.

Wang, Q., Smith, S. M., \& Huang, J. (2022). Origins of strigolactone
and karrikin signaling in plants. \emph{Trends in Plant Science, 27}
(5), 450-459.

Wang, S., Chen, A., Xie, K., Yang, X., Luo, Z., Chen, J., . . . Xu, G.
(2020). Functional analysis of the OsNPF4.5 nitrate transporter reveals
a conserved mycorrhizal pathway of nitrogen acquisition in
plants.\emph{Proceedings of the National Academy of Sciences USA, 117}
(28), 16649-16659.

Wang, T., Guo, J., Peng, Y., Lyu, X., Liu, B., Sun, S., \& Wang, X.
(2021). Light-induced mobile factors from shoots regulate
rhizobium-triggered soybean root nodulation. \emph{Science, 374} (6563),
65-71.

Wang, X., Chen, K., Zhou, M., Gao, Y., Huang, H., Liu, C., . . . Li, X.
(2022). GmNAC181 promotes symbiotic nodulation and salt tolerance of
nodulation by directly regulating GmNINa expression in soybean.\emph{New
Phytologist, 236} (2), 656-670.

Wen, A., Havens, K. L., Bloch, S. E., Shah, N., Higgins, D. A.,
Davis-Richardson, A. G., . . . Temme, K. (2021). Enabling Biological
Nitrogen Fixation for Cereal Crops in Fertilized Fields. \emph{ACS
Synthtic Biology, 10} (12), 3264-3277.

Williams, A., \& de Vries, F. T. (2020). Plant root exudation under
drought: implications for ecosystem functioning. \emph{New Phytologist,
225} (5), 1899-1905.

Wipf, D., Krajinski, F., van Tuinen, D., Recorbet, G., \& Courty, P. E.
(2019). Trading on the arbuscular mycorrhiza market: from arbuscules to
common mycorrhizal networks. \emph{New Phytologist, 223} (3), 1127-1142.

Wolinska, K. W., Vannier, N., Thiergart, T., Pickel, B., Gremmen, S.,
Piasecka, A., . . . Hacquard, S. (2021). Tryptophan metabolism and
bacterial commensals prevent fungal dysbiosis in Arabidopsis
roots.\emph{Proceedings of the National Academy of Sciences USA, 118}
(49).

Xie, X., Lai, W., Che, X., Wang, S., Ren, Y., Hu, W., . . . Tang, M.
(2022). A SPX domain-containing phosphate transporter from Rhizophagus
irregularis handles phosphate homeostasis at symbiotic interface of
arbuscular mycorrhizas. \emph{New Phytologist, 234} (2), 650-671.

Xie, X., Lin, H., Peng, X., Xu, C., Sun, Z., Jiang, K., . . . Zhao, B.
(2016). Arbuscular Mycorrhizal Symbiosis Requires a Phosphate
Transceptor in the Gigaspora margarita Fungal Symbiont. \emph{Molecular
Plant, 9} (12), 1583-1608.

Xu, L., Naylor, D., Dong, Z., Simmons, T., Pierroz, G., Hixson, K. K., .
. . Coleman-Derr, D. (2018). Drought delays development of the sorghum
root microbiome and enriches for monoderm bacteria. \emph{Proceedings of
the National Academy of Sciences USA, 115} (18), E4284-E4293.

Xue, L., Klinnawee, L., Zhou, Y., Saridis, G., Vijayakumar, V., Brands,
M., . . . Bucher, M. (2018). AP2 transcription factor CBX1 with a
specific function in symbiotic exchange of nutrients in mycorrhizal
Lotus japonicus. \emph{Proceedings of the National Academy of Sciences
USA, 115} (39), E9239-E9246.

You, Y., Kerner, P., Shanmugam, S., \& Khodakovskaya, M. V. (2023).
Emerging investigator series: differential effects of carbon nanotubes
and graphene on the tomato rhizosphere microbiome. \emph{Environmental
Science: Nano, 10,} 1570-1584.

Yu, N., Luo, D., Zhang, X., Liu, J., Wang, W., Jin, Y., . . . Wang, E.
(2014). A DELLA protein complex controls the arbuscular mycorrhizal
symbiosis in plants. \emph{Cell Research, 24} (1), 130-133.

Zboralski, A., Saadia, H., Novinscak, A., \& Filion, M. (2022).
Interplay between Arabidopsis thaliana genotype, plant growth and
rhizosphere colonization by phytobeneficial phenazine-producing
Pseudomonas chlororaphis. \emph{Microorganisms, 10} (3), 660.

Zeng, T., Rodriguez-Moreno, L., Mansurkhodzaev, A., Wang, P., van den
Berg, W., Gasciolli, V., . . . Limpens, E. (2020). A lysin motif
effector subverts chitin-triggered immunity to facilitate arbuscular
mycorrhizal symbiosis. \emph{New Phytologist, 225} (1), 448-460.

Zhang, B., Wang, M., Sun, Y., Zhao, P., Liu, C., Qing, K., . . . Wang,
X. (2021). Glycine max NNL1 restricts symbiotic compatibility with
widely distributed bradyrhizobia via root hair infection. \emph{Nature
Plants, 7} (1), 73-86.

Zhang, W., \& Mason, G. A. (2022). Modulating the rhizosphere microbiome
by altering the cocktail of root secretions. In: Oxford University
Press.

Zhao, X., Yuan, X., Xing, Y., Dao, J., Zhao, D., Li, Y., . . . Wang, Z.
(2023). A meta-analysis on morphological, physiological and biochemical
responses of plants with PGPR inoculation under drought
stress.\emph{Plant, Cell \& Environment, 46} (1), 199-214.

Zhou, J.-Y., Yuan, J., Li, X., Ning, Y.-F., \& Dai, C.-C. (2016).
Endophytic bacterium-triggered reactive oxygen species directly increase
oxygenous sesquiterpenoid content and diversity in Atractylodes
lancea.\emph{Applied and Environmental Microbiology, 82} (5), 1577-1585.

Zhou, X., Wang, J., Liu, F., Liang, J., Zhao, P., Tsui, C. K., \& Cai,
L. (2022). Cross-kingdom synthetic microbiota supports tomato
suppression of Fusarium wilt disease. \emph{Nature Communications, 13}
(1), 7890.

Zhou, Y., Ge, S., Jin, L., Yao, K., Wang, Y., Wu, X., . . . Foyer, C. H.
(2019). A novel CO 2-responsive systemic signaling pathway controlling
plant mycorrhizal symbiosis. \emph{New Phytologist, 224} (1), 106-116.

Zihalirwa Kulimushi, P., Arg\selectlanguage{ngerman}üelles Arias, A., Franzil, L., Steels, S.,
\& Ongena, M. (2017). Stimulation of fengycin-type antifungal
lipopeptides in Bacillus amyloliquefaciens in the presence of the maize
fungal pathogen Rhizomucor variabilis. \emph{Frontiers in Microbiology,
8} , 850.

\emph{}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

\textbf{Fig. 1: Microbiomes serve as the foundation for one health:} The
health of plants, humans, and the environment are interconnected and
rely on close association with microbial communities. The beneficial
microbial microbes in the plant rhizosphere determine plant productivity
by assisting in seed germination, foraging for nutrients under
nutrient-limiting conditions, or nutrient recycling along with providing
abiotic and biotic stress tolerance through production metabolites and
modulating host immunity respectively. In humans, the beneficial
microbes introduced via direct consumption of plant products or indirect
exposure through the environment contribute to overall health
maintenance by boosting the immune system against pathogens, reducing
the usage of antimicrobial compounds, and providing some essential
nutrients. The beneficial microbes can offer a sustainable solution for
the conservation of nature by replacing chemical fertilizers and
pesticides responsible for global warming and environmental
pollution\textbf{.}

\textbf{Hosted file}

\verb`image2.emf`  available at \url{https://authorea.com/users/297143/articles/732907-tailoring-beneficial-microbe-plant-interactions-for-one-health-benefits}

\textbf{Fig. 2: Mechanisms for plant-microbe interactions.}Plant/microbe
interactions occur in spermoshere, rhizosphere, and phyllosphere.
Microbes in the spermosphere aid seedling establishment by controlling
germination and the secretion of compounds that inhibit competing
pathogenic microbes. The plant/microbe chemical communication network
involves primary and secondary metabolites that attract beneficial
microbes and restrict pathogenic microbes. Beneficial microbes secret
allelochemicals with biocontrol activity. Phytohormones including indole
acetic acid (IAA), cytokinin (CK), gibberellic acid (GA), strigolactone
(SL), and salicylic acid (SA) are secreted by both plants and microbes.
Soil microbes not only enhance plant immunity by triggering systemic
resistance responses via MAMP-triggered immunity or effector-triggered
immunity, but they also directly inhibit invading pathogens. Beneficial
microbes can successfully evade plant immune surveillance by deploying
effector proteins to suppress plant immune response (A). The
microbe-derived PAMPs and MAMPs are perceived by
plasma-membrane-localized pattern-recognition receptors (PRRs) that
trigger signaling events including Ca influx, activation of plasma
membrane-bound NADPH oxidases (RBOH) that produce reactive oxygen
species (ROS burst). Oscillations in calcium concentrations (calcium
spiking) and ROS waves act together with a network of signalling
proteins as well as Ca-dependent protein kinases (CDPKs, CCaMKs and
CIPKs) to control transcriptional reprogramming, activation of
defense-related genes, secondary metabolite production, and defence
hormone synthesis. This system triggers immune response throughout the
plant resulting in systemic acquired resistance (B). Current concepts
concerning this signalling cascade are described in detail in the
accompanying text.

\textbf{Hosted file}

\verb`image3.emf`  available at \url{https://authorea.com/users/297143/articles/732907-tailoring-beneficial-microbe-plant-interactions-for-one-health-benefits}

\par\null

\textbf{Fig. 3: Genetic approaches to broaden the host range of
beneficial microbes.} Microbe-derived effector proteins can be
engineered to block host defenses and initiate symbiosis (A). Genetic
engineering approach to recreate nodule organogenesis in non-legume
plants. The Myc-receptor, which recognizes AMF-produced Myc-factors, has
been engineered to perceive Nod factors by replacing the outer domain of
the receptor. This induces the formation of nodule-like structures by
activating a common symbiotic signaling pathway (CSSP) (B). Another
approach is to facilitate the association between nitrogen-fixing
microbes and cereals including rhizopine synthesis in plants such as
wheat and rice. Rhizopine is sensed by nitrogen-fixing bacteria via
biosensor plasmids that encode rhizopine-binding proteins and
rhizopine-dependent transcription factors (TF). These proteins drive the
downstream expression of genes encoding proteins required for nitrogen
fixation (C). Finally, the recruitment of root-associated microbiota is
dependent on host genetics. Genome wide association study mapping will
identify novel host genetic loci that control microbial selection to
facilitate breeding efforts to improve crop resilience (D).

\textbf{Hosted file}

\verb`image4.emf`  available at \url{https://authorea.com/users/297143/articles/732907-tailoring-beneficial-microbe-plant-interactions-for-one-health-benefits}

\textbf{Fig. 4: Holobiont approaches for next-generation
agriculture.}Beneficial microbes can reduce the agricultural use of
fertilizers and chemical pesticides, and contribute to rhizosphere
carbon sink capacity (A). Rhizosphere microbiomes from plants inhabiting
extreme environments or stress-tolerant cultivars and can be
transplanted can be used in phytoremediation and soil improvement
approaches (B). Synthetic microbial communities (SynCom) can augment
crop quality. High quality crop production systems can be used to source
SynComs. High-throughput sequencing and systems biology approaches can
be used to identify appropriate SynCom systems. Network analysis
provides information on core microbial taxa and hubs and facilitates the
selection of best candidate microbes for further screening. The efficacy
and ecological impacts of SynComs must be validated in field studies
(C). Composites of the signaling chemicals found in root exudates
including flavonoids, \selectlanguage{greek}γ-\selectlanguage{english}aminobutyric acid, malate, and citrate can be
applied to soils to attract beneficial microbes (D). Nanomaterial-based
approaches are also an attractive approach for improving plant health by
releasing trapped soil nutrients and modulating root exudates (E).

\selectlanguage{english}
\FloatBarrier
\end{document}

