Mycorrhizal symbiosis alleviates plant water deficit within and across plant generations via plasticity

Abstract

SummaryPhenotypic plasticity is essential for organisms to adapt to local ecological conditions. Little is known about how mutualistic interactions, such as arbuscular mycorrhizal (AM) symbiosis, mediate plant phenotypic plasticity and to what extent this plasticity may be heritable (i.e. transgenerational effects).We tested for plant plasticity within- and across-generations in response to AM symbiosis and varying water availability in a full factorial experiment over two generations, using the perennial apomictic herb Taraxacum brevicorniculatum. We examined changes in phenotype, performance, and AM fungal colonization of the offspring throughout plant development.AM symbiosis and water availability triggered phenotypic changes during the life cycle of plants. Additionally, both triggered adaptive transgenerational effects, especially detectable during the juvenile stage. Drought stress and absence of AM fungi caused concordant plant phenotypic modifications towards a “stress-coping phenotype” within-and across-generations. Offspring’s AM fungal colonization was also affected by the parental environment.AM symbiosis can trigger transgenerational effects, including changes in functional traits related to resource-use acquisition and AM fungal colonization of the offspring, in turn affecting the biotic interaction. Thus, transgenerational effects of mycorrhizal symbiosis are not limited to plant fitness, but also improve plants’ ability to cope with environmental stress.

Competition‐induced transgenerational plasticity influences competitive interactions and leaf decomposition of offspring

“…This suggests that embryo modifications were not the only mechanism driving our observed transgenerational effects and points to other mechanisms, such as heritable epigenetic modifications or hormonal balance in embryos (Herman & Sultan, 2011; Rottstock et al ., 2017). Also, even though any parental effects are likely to fade away with time (Dechaine et al ., 2015; Puy et al ., 2020b), the effects associated with differences in seed mass seem to fade away faster (Latzel et al ., 2010). Meanwhile, the effect of seed mass on growth rate lasted until the 24 th day (i.e.…”

“…The later, transgenerational phenotypic plasticity – in short, transgenerational plasticity – occurs when the phenotype of progeny is influenced by the environmental conditions experienced by the parents (also referred to as parental or transgenerational effects; Herman et al ., 2014; Turcotte & Levine, 2016). The great majority of existing studies on transgenerational plasticity focus on phenotypic responses to abiotic factors (Galloway & Etterson, 2007; Auge et al ., 2017; Bej & Basak, 2017; Puy et al ., 2020a) and have generally overlooked the role of biotic interactions (Alonso et al ., 2019; Puy et al ., 2020b), such as competition between organisms. However, these biotic interactions are considered leading factors for controlling species coexistence, biodiversity maintenance, and ecosystem functioning (Van der Putten et al ., 2013; Kraft et al ., 2015; Valladares et al ., 2015).…”

“…In turn, individuals with conservative phenotypes, characterized by higher root biomass allocation and more structural and tougher tissues (i.e. low SLA, high LDMC, low SRL) are usually superior when resources are scarce (Reich, 2014; Díaz et al ., 2016; Puy et al ., 2020b). When there is an appropriate response towards well‐adapted phenotypes, phenotypic plasticity can increase species fitness and promote adaptation.…”

How do arbuscular mycorrhizas affect reproductive functional fitness of host plants?

“…Direct effects include increasing seed size or nutrients stored in endosperm, and indirect effects include that changing the trait plasticity of parental plant, which may lead to transgenerational transmission of phenotypic plasticity in functional adaptation (Herman and Sultan, 2011;Varga et al, 2013;Varga and Kytöviita, 2014;Yin et al, 2019). It is noteworthy that the transgenerational effect can operate via two mutually non-exclusive mechanisms, seed provisioning (seed size, seed nutritional quality, or hormonal balance), and environmentally induced heritable epigenetic modifications in offspring (Puy et al, 2022). Here, we review the effects of AM symbiosis on female functional fitness of host plants from two aspects: the effects of AM symbiosis on seed germination and the growth performance of germinated seedlings.…”

Soil Health and Biodiversity Is Driven by Intensity of Organic Farming in Canada

“…The greater legume content, and lower readily available soil P status, on organic dairy farms was also associated with greater forage legume root colonization by mycorrhizae (AMF) and a shift in AMF community composition, along with greater legume biological N 2 fixation (Schneider et al, 2015(Schneider et al, , 2017a. A fascinating recent study (Puy et al, 2021) has shown that plant phenotypic changes incurred by water availability and by parent plant AMF association, is transferred to the next generation of plants, thus conferring environmental stress resiliency across plant generations. One can speculate thus that enhanced crop resiliency to climate stresses often observed on organic farms is due to some degree to greater AMF and other beneficial plant-soil microbe interactions.…”