Plant-microbe interactions in the phyllosphere: facing challenges of the anthropocene

Abstract

Global change is a defining feature of the Anthropocene, the current human-dominated epoch, and poses imminent threats to ecosystem dynamics and services such as plant productivity, biodiversity, and environmental regulation. In this era, terrestrial ecosystems are experiencing perturbations linked to direct habitat modifications as well as indirect effects of global change on species distribution and extreme abiotic conditions. Microorganisms represent an important reservoir of biodiversity that can influence macro-organisms as they face habitat loss, rising atmospheric CO2 concentration, pollution, global warming, and increased frequency of drought. Plant-microbe interactions in the phyllosphere have been shown to support plant growth and increase host resistance to biotic and abiotic stresses. Here, we review how plant-microbe interactions in the phyllosphere can influence host survival and fitness in the context of global change. We highlight evidence that plant-microbe interactions (1) improve urban pollution remediation through the degradation of pollutants such as ultrafine particulate matter, black carbon, and atmospheric hydrocarbons, (2) have contrasting impacts on plant species range shifts through the loss of symbionts or pathogens, and (3) drive plant host adaptation to drought and warming. Finally, we discuss how key community ecology processes could drive plant-microbe interactions facing challenges of the Anthropocene.

Leaf bacterial microbiota response to flooding is controlled by plant phenology in wheat (Triticum aestivum L.)

“…These studies revealed that the leaf microbiota was characterized by season-specific bacterial taxa, thus inferring on particular mechanisms of leaf adaptation at different plant growth stages 33 , 34 . Collectively, these findings support the central role of plant phenology in leaf microbiota assembly, and the likelihood of functional and evolutionary changes associated with these predictable patterns 35 , 36 .…”

Bacterial Microbiome in the Phyllo-Endosphere of Highly Specialized Rock Spleenwort

“…By affecting traits of their host plants positively, some endophytic microorganisms, e.g., bacteria and fungi, support the functionality of ecological networks and the evolutionary success of land plants ( Vandenkoornhuyse et al, 2015 ; Chen et al, 2020 ; Compant et al, 2020 ; Harrison and Griffin, 2020 ; Lyu et al, 2021 ; Tan et al, 2021 ). Furthermore, endophytic microbiomes have been increasingly considered to be treasure chests to discover bioactive metabolites ( Gouda et al, 2016 ; Ek-Ramos et al, 2019 ; Wu et al, 2021 ; Cernava and Berg, 2022 ), to promote sustainable agriculture ( Chen Q. L. et al, 2021 ; French et al, 2021 ), and to counteract the impact of the global climate change ( Suryanarayanan and Shaanker, 2021 ; Perreault and Laforest-Lapointe, 2022 ). Unfortunately, the holobiome of the vast majority of plants is still awaiting to be discovered, which applies particularly to the bacterial diversity in the endo-phyllosphere—meaning the niche spaces inside the leaves of land plants ( Vorholt, 2012 ; Khare et al, 2018 ; Cordovez et al, 2019 ; Harrison and Griffin, 2020 ; Chaudhry et al, 2021 ; Hawkes et al, 2021 ; Chialva et al, 2022 ).…”

Disentangling leaf-microbiome interactions in Arabidopsis thaliana by network mapping

“…Experimental studies have demonstrated that the phyllosphere harbors diverse microbial communities that in uenced ecosystem functioning [14][15][16][17][18][19]. Recent studies stress the importance of understanding the mechanisms underlying how plant-microbe interactions in the phyllosphere could in uence host survival and tness in the context of global change [20,21]. Several studies have illustrated that host genotypes can in uence the composition of the leaf microbiome [22][23][24], but little is clear how the plant shapes its leaf microbiota and how the leaf microbiome contributes to plant phenotypic traits [25][26][27].…”