2.2 Wired connections between independent plants via
Dodder-mediated interspecific signaling
Dodders (Cuscuta spp.) are plant holoparasites that acquire water
and nutrients from host plants via the haustorium, which physically
connects the parasite to its host. Dodder species have broad host range,
and can interconnect several plant species or clusters of the same
species (Figure 1) to generate a common dodder network. The common
dodder network can be considered as an inter-plant highway that
translocates large numbers of proteins, RNA, metabolites, and plant
viruses over a distance of at least 100 cm (Hettenhausen et al. ,
2017, Zhuang, Li, Song, Hettenhausen, Schuman, Sun, Zhang, Li, Song &
Wu, 2018). The common dodder network can translocate more than 1,500
proteins between soybean and Arabidopsis, and some of these proteins can
localize in dodder seeds. Approximately 15–30% of dodder proteins have
host origin, including transcription factors and R proteins that may
function in signal transaction. Dodder proteins can transfer to host
plant cells.
Plants can anticipate future threats by receiving neighboring plant
signals transferred through the common dodder network. Although there
are few reports on the role of the common dodder network in inter-plant
signaling, the results indicate that these transferred signals are
important in biotic/abiotic stress responses. When a host of the dodder
plant is under abiotic stress such high salinity, dodder transfers
salinity stress signals through a cluster of plants at a rate of 1.2 cm
per min, which prime salt tolerance in neighboring receiver plants. This
receiver plant priming changes the transcriptome, proline levels, and
stomatal conduction, so that the receiver plant stress response becomes
similar to that of the donor plant (Li, Zhang, Liu, Liu, Shen, Zhuang &
Wu, 2020b).
Plants infected with different herbivorous insects transfer relatively
long-distance signals to conspecific and heterospecific neighbors via
the common dodder network (Hettenhausen et al. , 2017, Zhuanget al. , 2018). Myzus persica infestation reduces the
contents of salicylic acid (SA) and jasmonic acid (JA) in dodder
(Cuscuta australis ) by up to 58% and 41%, respectively. Aphids
can modulate hormonal signaling by injecting effector proteins into
dodder plants (Rodriguez & Bos, 2013). Aphid-infested dodder induce JA
but not SA in soybean hosts, and subsequent phloem sap feeding byM. persica and chewing by Spodoptera litura causes 41%
and 20% less damage, respectively, in dodder-infected plants than in
control plants. Dodder transfers signals from insect-damaged soybean to
conspecific or heterospecific plants, such as tomato and Arabidopsis.
Gene expression and RNA-seq analyses reveal intense transcriptome
modification in receiver plants. An unknown signal can translocate
between common dodder network–connected Arabidopsis plants at a rate of
1 cm/min. A wave of signal transduction propagated between connected
Arabidopsis plants, as intracellular WRKY 40 and WRKY53 transcription
factors reached maximum expression at 45 and 90 min after donor plant
damage in the second and fourth plants in the cluster, respectively
(Zhuang et al. , 2018).