Introduction
Soil
microbes have been highlighted as a candidate factor driving plant
diversity-productivity relationships (Chen et al. 2019; Lianget al. 2019; Jia et al. 2020; van Ruijven et al.2020). The majority of experimental studies testing this idea have
compared plant diversity-productivity relationships in live versus
sterilized soils (Maron et al. 2011; Luo et al. 2016), or
through inoculating sterile substrates with different microbial guilds
(Klironomos et al. 2000; Schnitzer et al. 2011). In
natural ecosystems, however, plant diversity can influence intact soil
biota and abiotic properties through biochemically diverse litter
production and root exudates (Stephan et al. 2000; Kowalchuket al. 2002; Millard & Singh 2010; Milcu et al. 2013;
Mommer et al. 2018), and this soil legacy can feed back to
influence subsequent plant communities, leading to so-called
“plant-soil feedbacks” (PSFs) (Bever 1994; van der Putten et
al. 2013). To date, experimental evidence illuminating the influence of
soil microbes on plant diversity-productivity relationships through PSFs
remains limited (but see Jing et al. 2015; Wang et al.2019; Jia et al. 2020).
Soil pathogens can contribute to plant diversity-productivity
relationships by enhancing the appearance of a complementarity effect
(niche differentiation and facilitation among species, CE) via negative
density dependence. Here, if plant performance is reduced in
monocultures due to accumulation of species-specific soil pathogens,
then plants are likely to perform better in multiple-species mixtures
due to dilution of pathogenic effects (Maron et al. 2011;
Schnitzer et al. 2011; Mommer et al. 2018; van Ruijvenet al. 2020). Soil mutualists could contribute to diversity
effects as well, through enhancing resource partitioning in mixtures, as
plant communities with high richness might host diverse mutualist
communities and different guilds have different host effects (Maherali
& Klironomos 2007; Wagg et al. 2011; Jing et al. 2015;
Wang et al. 2019; Jia et al. 2020). Soil microbes are
likely to also influence the selection effect (the likelihood of the
presence of a particular productive plant species increases in a
species-rich community, SE), as particular microbial guilds (e.g.,
species-specific pathogens and mutualists) will enhance or reduce the
dominance of a particular plant species in mixtures (Vogelsang et
al. 2006; Wagg et al. 2011; Walder et al. 2012). It is
the prerequisite of soil microbe-mediated biodiversity effects that soil
microbial assemblages and the strength of PSFs differ among plant
species richness levels (Mommer et al. 2018), but the
experimental test for this assumption is lacking.
There is currently growing evidence that drought can alter soil abiotic
and biotic properties, mainly through two non-exclusive mechanisms: 1)
specialized soil pathogens become dormant under drought stress, and they
are subsequently reactivated by rewetting (Kaisermann et al.2017; Meisner et al. 2018), meaning plant communities under
drought receive a reprieve from pathogens; 2) plants select for
mycorrhizal fungi guilds which promote plant efficiency of soil water
capture under drought stress (Querejeta et al. 2009; Mariotteet al. 2017). Consequently, drought can generate a soil microbial
legacy that has long-lasting effects on subsequent plant communities (de
Vries et al. 2012; Kaisermann et al. 2017; De Longet al. 2019). However, little is known about how drought and
plant diversity interact to cause combined soil legacy effects on plant
performance and biodiversity-productivity relationships.
Plant diversity and drought-induced soil legacy could interact with
subsequent drought events to regulate plant performance. For example,
drought could simply weaken soil legacy effects/feedbacks on future
plants and shift PSFs from positive and negative to neutral (Fryet al. 2018; Snyder & Harmon-Threatt 2019). Previous studies
also suggest that plant drought resistance is enhanced when growing in
conspecific soil with legacy of historical drought events (de Vrieset al. 2012; Lau & Lennon 2012; Allsup & Lankau 2019). However,
these studies tested single plant species, but how soil legacy of plant
diversity and drought interact with subsequent soil moistures to
influence diversity effects remains unexplored.
Here, we performed plant diversity-productivity relationship experiments
under drought and ambient conditions over two phases (Fig. 1). In the
conditioning phase (Phase I), plant communities with a range of species
richness levels grew in homogeneous soils, and soil microbial
communities were trained by these plants. In the response phase (Phase
II), newly-established plant communities grew with soil inoculums which
the same plant communities conditioned. Drought was manipulated in both
phases to stimulate drought legacy effects and to assess responses to
drought from these legacy effects. We addressed two key research
questions: 1) Does plant diversity and drought cause soil legacy effects
through influencing soil microbial communities? (2) How does this soil
microbial legacy regulate plant diversity-productivity relationships?