Shaping the leaf microbiota: plant–microbe–microbe interactions

Abstract

The aerial portion of a plant, namely the leaf, is inhabited by pathogenic and non-pathogenic microbes. The leaf's physical and chemical properties, combined with fluctuating and often challenging environmental factors, create surfaces that require a high degree of adaptation for microbial colonization. As a consequence, specific interactive processes have evolved to establish a plant leaf niche. Little is known about the impact of the host immune system on phyllosphere colonization by non-pathogenic microbes. These organisms can trigger plant basal defenses and benefit the host by priming for enhanced resistance to pathogens. In most disease resistance responses, microbial signals are recognized by extra- or intracellular receptors. The interactions tend to be species-specific and it is unclear how they shape leaf microbial communities. In natural habitats, microbe-microbe interactions are also important for shaping leaf communities. To protect resources, plant colonizers have developed direct antagonistic or host manipulation strategies to fight competitors. Phyllosphere-colonizing microbes respond to abiotic and biotic fluctuations and are therefore an important resource for adaptive and protective traits. Understanding the complex regulatory host-microbe-microbe networks is needed to transfer current knowledge to biotechnological applications such as plant-protective probiotics.

Protective host-dependent antagonism amongPseudomonasin theArabidopsisphyllosphere

“…Further advancements in understanding of the plant-microbe-microbe complex in the light of plant health can improve our agriculture practices, allowing the development of more sustainable plant protection methods [39][40][41].…”

Temporal and spatial changes in phyllosphere microbiome of acacia trees growing in arid environments

“…This might explain ndings from other studies where diversity was higher for endophytic microbiomes. In our case, however, both A. raddiana and A. tortilis had a lower endophytic bacterial diversity compared to epiphytic bacterial diversity throughout the sampling regime (Table S4); the lower diversity of endophytic microbial communities compared to epiphytic communities may be a result of plant stress and physiological conditions regulated by stomatal opening [38,39]. In fact, Chao1 richness in epiphytic microbial communities in A. raddiana and A. tortilis was higher in January, March and November compared to summer months and corresponded to plant water vapour pressure de cit (VPD) stressing the importance of the physiological state of the plant in shaping endophytic bacterial communities (Fig.…”

Induced systemic resistance impacts the phyllosphere microbiome through plant-microbe-microbe interactions

“…Notably, we focused on the bacterial part of the microbiome, and cannot exclude possible additional effects of e.g. fungi and other eukaryotic microbes (Chaudhry et al, 2020).…”

“…Notably, the phyllosphere microbiome of WCS417-treated plants displayed a significantly reduced species richness. Because lower richness in microbiota has been associated with a lower stability of the microbiome and a higher risk of dominance by pathogens (Chaudhry et al, 2020; Tao Chen et al, 2020; Ives & Hughes, 2002), this suggests a possible trade-off of ISR in plants. In this respect, it seems of interest that we detected considerably less significant shifts in the phyllosphere microbiome composition than Chen et al (2020), who studied the influence of local immune response driven by pathogen-associated molecular patterns (PAMPs).…”

“…Local interactions of plant organs with pathogens can trigger long-distance signalling, for example from leaves to roots, and mediate changes in root exudates that influence the composition of the rhizosphere microbiota (Berendsen et al, 2018;Rudrappa, Czymmek, Pare, & Bais, 2008;Yu, Pieterse, Bakker, & Berendsen, 2019). Similar changes in the plant immune status are associated with the dynamics of the phyllosphere microbiome (Chaudhry et al, 2020). Certain commensal bacteria from the phyllosphere, in turn, have been shown to enhance, for example, SA-associated immunity (Vogel, Bodenhausen, Gruissem, & Vorholt, 2016).…”