Beneficial and pathogenic plant-microbe interactions during flooding stress

Abstract

The number and intensity of flood events will likely increase in the future, raising the risk of flooding stress in terrestrial plants. Understanding flood effects on plant physiology and plant-associated microbes is key to alleviate flooding stress in sensitive species and ecosystems. Reduced oxygen supply is the main constrain to the plant and its associated microbiome. Hypoxic conditions hamper root aerobic respiration and, consequently, hydraulic conductance, nutrient uptake, and plant growth and development. Hypoxia favours the presence of anaerobic microbes in the rhizosphere and roots with potential negative effects to the plant due to their pathogenic behaviour or their soil denitrification ability. Moreover, plant physiological and metabolic changes induced by flooding stress may also cause dysbiotic changes in endosphere and rhizosphere microbial composition. The negative effects of flooding stress on the holobiont (i.e., the host plant and its associated microbiome) can be mitigated once the plant displays adaptive responses to increase oxygen uptake. Stress relief could also arise from the positive effect of certain beneficial microbes, such as mycorrhiza or dark septate endophytes. More research is needed to explore the spiralling, feedback flood responses of plant and microbes if we want to promote plant flood tolerance from a holobiont perspective.

Keywords: flood resilience; holobiont; inundation; pathogens; phyllosphere; plant endophytes; rhizosphere; waterlogging.

Figure 1

Main physiological changes experienced by plants during flooding stress. Oxygen (O₂) depletion is the main direct effect produced by flooding. Poor soil aeration alters root energy metabolism due to the inhibition of the TCA cycle in the mitochondria and the stimulation of glycolysis and fermentation, which leads to the accumulation of toxic ethanol in roots. Hypoxia also leads to the inhibition of the aquaporin activity, which together with the altered root metabolism, contribute to stop the formation and elongation of lateral roots. Alterations in root functioning rapidly extend to the aerial parts, with hydraulic and chemical signals dominating the root to shoot communication. Low aquaporin activity and increased resistance to apoplastic water movement reduce xylem conductivity and, together with abscisic acid (ABA) accumulation in the leaves, enhance stomatal closure. Stomatal closure and impaired photosynthesis reduce CO₂ uptake and the production of carbohydrates. Leaf chlorophyll concentration (chl) decreases due to photoinhibition and deficient root nitrogen uptake. The gaseous hormone ethylene is rapidly synthesised under hypoxic conditions in the roots, or in the leaves from its precursor ACC (1‐aminocyclopropane‐1‐carboxylate), causing leaf epinasty, reducing leaf growth, and inducing stomatal closure. Ethylene accumulation also leads to the formation of aerenchyma, which facilitates gas diffusion, suberin‐rich tissues, which prevent radial O₂ loss (ROL), and hypertrophied lenticels, adventitious roots and pneumatophores, which favour O₂ transport to submerged plant parts. Created with BioRender.com [Color figure can be viewed at wileyonlinelibrary.com]

Figure 2

Main flood effects on bulk soil and rhizosphere microorganisms. Low oxygen (O₂) conditions induced by flooding impact the rhizosphere and bulk soil microbial composition by producing a switch from aerobic to anaerobic microorganisms. The continuous flow of microbes from bulk soil to rhizosphere (indicated in the lower part of the diagram) can impact the taxonomic composition of the rhizosphere. One of the most important effects of soil microbiome alterations due to flooding is the variation in the nutritional status of the soil. Regarding nitrogen, the inhibition of nitrifying microorganisms and the consequent boost of denitrifiers induce the consumption of nitrate (NO₃ ⁻) and nitrite (NO₂ ⁻) to produce different gaseous nitrogen forms (NO, N₂O, and N₂). Nitrogen limitation may ultimately affect different aspects of plant growth. Hypoxic conditions on bulk soil also induce methanogenic processes due to the degradation of the soil organic matter by anaerobic methanogenic microbes. This process culminates with the production of methane (CH₄) and CO₂, which can be released to the atmosphere through soil or plant tissues. These changes on rhizosphere and soil microbes can be mitigated through specific plant adaptations favoring O₂ transport (e.g., aerenchyma). Plant stress can alter the composition of the root exudates and, therefore, produce a dysbiosis on the rhizosphere. Plant stress (and indirectly microbial stress) could be mitigated by the presence of specific groups of microbes, such as the plant growth promoting rhizobacteria (PGPR), which cleaves the ethylene precursor ACC (1‐aminocyclopropane‐1‐carboxylate) through the release of ACC‐deaminases. Created with BioRender.com [Color figure can be viewed at wileyonlinelibrary.com]

Figure 3

Main flood effects on plant endosphere microbiome, including the root system and the aerial part of the plant. Low oxygen (O₂) conditions induced by flooding impact the root microbiome by producing a switch from aerobic to anaerobic microorganisms. Alterations of the chemical composition of the root system due to the activated fermentative pathways, and the reduced growth of the root system due to hypoxia or ethylene synthesis, produced dysbiotic changes on the microbial community composition of the root system. These dysbiotic changes are usually produced by the increase in the competitive ability of certain microbes, i.e. oomycete pathogens or ethanol‐catabolizing microorganisms, and the inhibition of the presence of beneficial aerobes such as endophyte or mycorrhizal fungi. Variations on root system architecture may also cause adjustments in the root microbial community, with a probable reduction in the richness and diversity of species due to low nutrient provision. The extent to which new developed adventitious roots contribute to alterations on the root microbiome remains unknown. Furthermore, the signals generated on the root system, especially the diffusible ones such as ethylene or methane (CH₄), can affect the phyllosphere microbiome by inhibiting bacterial symbiosis or enhancing the presence of Methylobacterium, a bacterial genus with the ability to use CH₄ as a carbon source. Root adaptations induced by the synthesis and signalling of ethylene, such as adventitious roots, radial oxygen loss (ROL) barriers and aerenchyma attenuates flooding (hypoxic) stress on root microbial composition. Futhermore, the presence of certain microbes can improve flooding stress tolerance by enhancing aerenchyma formation (as in the case of the fungi Phomopsis liquidambari) or the development of ROL barriers (as in the case of certain anaerobic microbes). Microbes producing ACC‐deaminase can mitigate ethylene stress. Other endophytes, such as dark septate endophytes (DSE), can increase root growth by enhancing nutrient uptake and ameliorating the plant antioxidant response. Created with BioRender.com [Color figure can be viewed at wileyonlinelibrary.com]

Figure 4

Increased tree mortality in a stream bank of a Quercus ilex forest in Extremadura, SW Spain, where flooding and the oomycete Phytophthora cinnamomi (Pc) co‐occur. (a) Image of the study site showing places of Pc isolation and distribution of living and dead trees. (b) Mean values of water table depth measured in stream banks and upper slopes from March 2009 to February 2011. Assuming sinker roots of Q. ilex growing deeper than 5 m (Moreno et al., 2005), about one‐third of the roots of trees located in stream banks would have been waterlogged for 4 months in 2010 and 2 months in 2011. Bars denote standard errors (n = 5 sites; adapted from Corcobado et al., 2013). (c) Fine roots of Q. ilex trees examined from soil pits (2.5 m wide and 1.5 m deep; n = 288) dug in upper slopes and stream banks. (d) Relative abundance of non‐vital, vital non‐mycorrhizal and vital ectomycorrhizal root tips of Q. ilex trees (n = 192) located in upper slopes and stream banks (n = 48; adapted from Corcobado et al., 2014b). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 5

Main direct and indirect flood effects experienced by the plant and its associated microbiome. Direct effects of flooding on the plant and the plant microbiome are mainly driven by hypoxic soil conditions. Flooding changes the normal plant aerobic metabolism into a fermentative metabolism involving enhanced carbohydrate consumption through glycolysis. A hormonal imbalance due to increase ethylene synthesis also occurs, leading to different detrimental processes in the plants such as the inhibition of photosynthesis. Plant physiological and metabolic alterations drive the plant‐associated microbiome (including the rhizosphere and the endosphere microbiome). These changes include modifications in xylem sap pH, alterations on the chemical composition of root tissues or root exudates due to the production of ethanol during fermentation or changes on carbohydrate content, which usually lead to negative microbial recruitments. Nevertheless, the root exudation of specific chemical components may enhance the recruitment of certain microbes that counteract some negative stress effects (“cry‐for‐help” mechanism). Alterations on the root system architecture (RSA), e.g., reflected in reduced root growth, can alter the plant microbiome diversity; the development of new adventitious roots has an unknown effect on microbial composition. On the other hand, hypoxic soil conditions induced by flooding promote the enrichment of anaerobic microbes, which are usually linked with processes such as fermentation, methanogenesis or denitrification. The presence of these microorganisms produces indirect negative effects on the plant, such as soil denitrification or the outcompetition of certain microbial members by others with pathogenic behaviour. Nevertheless, the persistence of some microbes under stress conditions may have beneficial effects for the plant during the stress. For example, the establishment of endophytes such as the dark septate endophytes (DSE) or the endophytic fungi Phomopsis liquidambari may be involved in enhancing root growth, by improving nutrient uptake, or in stimulating the formation of aerenchyma. Other symbiotic microbes such as the plant‐growth promoting rhizobacteria (PGPR) are able to synthesise the enzyme ACC‐deaminase that cleaves ACC and reduces ethylene synthesis. Created with BioRender.com