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Guided reading
Plants form complex interaction networks with different microbial communities in the environment, and the complex interactions between plants and their microbial communities can profoundly affect ecosystem processes and functions. The phyllosphere is the aerial part of the plant, which provides a unique habitat for a variety of microorganisms, and in turn, the phyllosphere microbial community also significantly affects the growth and development of plants. As an open system, the phyllosphere is subject to environmental perturbations, including global changes, that affect the interactions between plants and microbial communities. In this review, we aim to outline how global change will affect the complex interactions between the phyllosphere and its microbiota, and to identify some priority areas for future research.
Paper ID
原名：Impacts of global change on phyllosphere microbiome
原名： The impact of global change on phyllosphere microbial communities
Journal : New Phytologist
IF：10.151
Release time: 2021.12.18
Corresponding author: Academician Zhu Yongguan
Corresponding Author Unit: Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences
DOI Number: https://doi.org/10.1111/nph.17928
Overview directory
1 Introduction
2 Ecological functions of phyllosphere microbial communities
3 Drivers and sources of phyllosphere microbial communities
4. Hotspots and frontier trends of foliar microbiota in response to global change
5 Effects of agricultural fertilization on the phyllosphere microbial community
6 The impact of global warming on phyllosphere microbial communities
7 Effects of precipitation and drought on phyllosphere microbial communities
8 Eco-evolutionary dynamics of phyllosphere and its microbial community under global climate change
9 Conclusions and viewpoints
main content
1 Introduction
Interactions between plants and their microbiota are critical for host performance and resilience to environmental perturbations such as global change. Previous studies on plant microbes have focused on the rhizosphere, including the symbiotic relationship between plant roots and bacteria and fungi and the dynamics of pathogenic bacteria in soil. In the past decade, with the advent of molecular and genomic technologies, the study of the plant microbiome has expanded rapidly, from the rhizosphere to the phyllosphere, inner layer, and seeds/fruits. The phyllosphere represents the aerial part of the plant, where a variety of microorganisms exist in both epiphytic (organisms that grow on the surface of the plant) and endophytic (organisms that live inside the plant) niches. Considering the upper and lower surfaces of leaves, the total leaf area on Earth is estimated to exceed 10 9 km 2 and contain as many as 10 26 bacterial cells. The Earth and its ecosystems are undergoing rapid global changes, such as climate change (such as warming and drought) and land use changes (such as habitat loss and fertilizers), which have influences of various interactions. A systematic understanding of how global change affects phyllosphere microbial communities can provide an important basis for harnessing the microbiota to promote ecosystem resilience and plant productivity in a sustainable manner . In this review, we aim to outline how global change will affect the complex interactions between the phyllosphere and its associated microbial communities , and to identify some priority areas for future research .
2 Ecological functions of phyllosphere microbial communities
Microbes that colonize the foliar play critical roles in a variety of functions (Figure 1), including plant productivity and fitness by affecting leaf function and longevity, seed quality, apical growth, flowering, and fruit development, while also removing play a key role in pollutants. For example, some foliar-dwelling plant growth-promoting bacteria, such as Microbacterium , Stenotrophomonas , and Methylobacterium , can produce natural growth regulators (such as indoleacetic acid) and Nitrogen fixation to improve growth and nutritional status of host plants. The foliar microbiota also plays an important role in reducing plant methanol (eg, methylotrophic bacteria) and isoprene (eg, isoprene-degrading bacteria Variovorax (R)) emissions to the atmosphere. In addition, the phyllosphere microbial community plays an important role in maintaining plant health and inhibiting the overgrowth of phytopathogens. For example, phyllosphere microbial communities can protect Arabidopsis plants from fungal pathogens and dysbiosis (disruption of microbial community homeostasis) that can have deleterious effects on host health. Recent studies have shown that bacteria and yeasts that colonize nectar can modulate the chemical composition of nectar, thereby affecting access/foraging by insect pollinators. Thus, the foliar microbiota contributes to the gut microbiota of insect pollinators, thereby affecting their health and behavior. Nonetheless, it should also be noted that foliar microbes may have negative effects on the host plant. In the phyllosphere, the presence of a large and diverse microbial community may increase its competition with plants for nutrients and water. Some members of the foliar microbiota may act as phytopathogens to cause different forms of plant disease. Recently, Zhou et al. reported that the foliar microbiota was involved in the spread of antibiotic resistance genes in urban greening. Another report suggests that phyllosphere microbial communities contribute to the establishment of the invasive plant black algae ( Hydrilla verticillata L.) under nitrogen-scarce conditions. There is growing evidence thatGlobal change has pervasive effects on plant health and ecosystem functioning, and harnessing the beneficial functions provided by phyllosphere microbial communities to enhance plant growth and adaptation to meet the challenges of global change is considered a viable and sustainable approach .
Fig. 1 Ecological functions of phyllosphere microbial communities.
3 Drivers and sources of phyllosphere microbial communities
Since the phyllosphere is an open system, its associated microbiota may originate from multiple sources. 1) complex and variable environmental conditions (such as temperature, solar radiation, humidity, soil type and agricultural activities) constrain the assembly of phyllosphere microbial communities, 2) plant species and genotypes, 3) specific leaf structures or resource secretions (e.g. leaf age and surface roughness, primary and secondary metabolites), 4) complex interactions between different trophic levels, such as microbe-microbe interactions and plant-herbivore-microbiota interactions. In addition, invasive plants caused by global change may affect phyllosphere microbial communities by altering soil properties and microbial communities, as well as plant-soil feedbacks. The phyllosphere microbial community composition is closely related to the surrounding environment of the host plant, such as soil, air and surrounding plants. For example, soil microbes can enter root tissue from new roots or wounds to form the root microbiota, and a portion of this can then be transferred to the aerial parts of plants (i.e., the phyllosphere) via the xylem and phloem systems. This may partly explain the phenomenon of microbial overlap between plant tissue and soil. In addition, the opening of leaf stomata and wounds provides a pathway for transformation and migration between endophytes and epiphytes, and provides opportunities for external microbial colonization of plants from aerosols and insects, which also suggests that plants and the environment are interacting with each other. Associated. However, a recent study analyzed the sources of phyllosphere microbes through a custom micro-world that can control external microbes, and showed that microbial sources from soil and air are limited. In another study, oak seeds were found to transmit most of the microbes to the root and leaf margins, underscoring that plant seeds are a reservoir of plant microbiota. Seeds can carry highly diverse and beneficial bacterial taxa to ensure optimal bacterial symbiosis in progeny. These studies highlight that the genetic properties of plant microbes may play a dominant role in shaping the phyllosphere microbiota .
In conclusion, the sources of phyllosphere microbes are complex and dynamic, influenced by plant intrinsic factors and environmental conditions, while biotic and abiotic selection pressures must also be considered. Therefore, one possible mechanism is that environmental and genetic factors together determine the assembly of microbial communities. Uncovering how global change affects microbial community assembly, sources of transmission, and interactions between plants and microbial communities can provide mechanistic insights into the regulation of microbial communities in the future.
4. Hotspots and frontier trends of foliar microbiota in response to global change
By retrieving citation data from the Web of Science Core Collection database, bibliometric analysis was performed to highlight the hotspots and frontier trends of the phyllosphere microbiota in response to global change. Keyword co-occurrence network analysis showed that research in recent years has mainly focused on the relationship between phyllosphere microbial communities and plant growth and health under global change scenarios. These relationships also included interactions between pathogens and plant disease resistance (Fig. 2a). The phyllosphere microbial community is under increasing pressure due to climate change (especially warming and drought). Climate change stress may lead to microbial community instability, in which reduction of beneficial taxa weakens plant resistance to pathogen invasion and disease development. In addition, the phyllosphere microbial community also participates in the carbon and nitrogen cycle through nitrogen fixation, metabolizing plant metabolites, and producing volatile organic compounds (VOCs), but the response of the phyllosphere microbial community-mediated carbon and nitrogen cycle to climate change is unclear. While the network suggests that the model plant Arabidopsis thaliana is the most popular object to study, there is an urgent need for a new, more agriculturally relevant plant model to study crop-microbiota interactions that could be developed for Effective microbial tools for sustainable agriculture. We further used Burst word detection analysis to reveal the temporal order pattern of keywords, and explored the trends and progress of phyllosphere microbial ecology research in response to global change in the past decade (Fig. 2b). The research on plant growth and stress resistance is the most powerful research field since 2018, and it is a research hotspot that is currently widely concerned . In recent years, the development of emerging technologies may be a driving factor for an increase in mechanistically relevant studies, allowing researchers to unravel the mechanisms by which phyllosphere microbial communities regulate plant growth and tolerance.
Figure 2 Quantitative analysis of literature on phyllosphere microbiota research from January 2010 to May 2021 based on the Web of Science Core Collection database. (a) Keyword co-occurrence network. Nodes represent unique keywords; node size is proportional to the number of references; node colors represent modules. (b) Burst word detection analysis. Length indicates burst state duration; color saturation indicates reference burst strength. Bibliometric analyses were performed by retrieving citation data based on subject searches, using N deposition or nitrogen deposition, CO2 or carbon dioxide, precipitation or temperature or climate change) and (foliar* or leaf) and (fungi* or bacteria* or Microorganisms* or Archaea* or Viruses or Protists* to query. Screening results included literature from January 2010 to May 2021, and further analyzed by CiteSpace to highlight hotspots and frontiers of phyllosphere microbial communities in response to global change trend.
5 Effects of agricultural fertilization on the phyllosphere microbial community
Modern agricultural production relies heavily on the use of chemical fertilizers such as nitrogen (N), phosphorus (P) and potassium (K) fertilizers. Global agricultural production is projected to increase by 70% by 2050 to feed a growing population, and the use of fertilizers in agricultural production is likely to increase substantially in the future. However, intensive fertilization can lead to soil degradation such as acidification and environmental pollution. At present, most studies on the effects of chemical fertilizers on the microbial community focus on the soil and rhizosphere, while there are few studies on the response of the phyllosphere microbial community to chemical fertilizers. Overall, bacterial, fungal, and protist diversity was lower in the phyllosphere compared to the soil and rhizosphere, and the alpha and beta diversity of these phyllosphere-associated microbes tended to show greater resistance to fertilization sex. One of the reasons may be due to the openness of the phyllosphere, and under the dynamic heterogeneity environment, the phyllosphere associated microorganisms are affected by various factors, which may weaken the effect of fertilization on the changes of phyllosphere microorganisms. Furthermore, a recent study of the soil-plant continuum in maize, wheat, and barley showed that host selection played a more important role than fertilization measures in shaping phyllosphere assembly and network complexity. However, the fertilization process can affect some specific microbial taxa within the phyllosphere. For example, excessive application of chemical N fertilizers increased the relative abundance of potentially pathogenic fungi in the inner layer of leaves. Similarly, a study in sorghum showed that long-term fertilization regimes had no significant effect on the diversity and composition of phyllozoa protozoa communities, but had significant effects on certain protozoa-consuming groups such as amoeba. In addition, other macro- and micro-nutrients also play a role in phyllosphere microbial community assembly. For example, the application of some nutrients increased soil microbial diversity, but decreased the relative abundance of the pathogen Ca. Liberibacter. Asiaticus in the phyllosphere of Gannan navel oranges . Although these studies provide valuable information, the fundamental understanding of the mechanisms of assembly and activity of phyllosphere microbial communities under fertilization is still in its infancy.
In addition to fertilization, microbial communities in agro-ecosystems are often influenced by agronomic management regimes such as organic and conventional management. Organic farming has been reported to increase the fungal diversity in the wheat phyllosphere compared to conventional management. A recent study also showed that agricultural management (i.e., organic, transformational, and conventional) strongly influenced the composition, function, and symbiotic network of sugarcane foliar microbial communities. Organic farming has a complex microbial network that enriches some plant growth-promoting bacteria, such as Bradyrhizobium and Bacillus , while conventional farming reduces functions involved in cell motility and energy metabolism in the phyllosphere microbial community gene abundance. Evidence suggests that agricultural management is an important factor driving the assembly of phyllosphere microbial communities. Uncovering the interaction between phyllosphere and microbial communities and their molecular mechanisms under different agricultural management styles can provide new scientific knowledge for utilizing phyllosphere microbial communities to promote plant productivity and sustainable agriculture.
6 The impact of global warming on phyllosphere microbial communities
Global warming caused by the greenhouse effect is expected to have a major impact on element cycling and the functioning of terrestrial ecosystems such as vegetation dynamics, which will greatly affect phyllosphere microbial communities (Fig. 3). According to the Intergovernmental Panel on Climate Change (IPCC2013), the global average surface temperature is expected to rise by 2-3°C over the next few decades, which will lead to an increase in the frequency and duration of global droughts.
In recent decades, experimental studies on the effects of climate warming have mainly focused on soil microbial communities, while the potential effects of climate warming on the abundance and composition of foliar microbiota have been mostly ignored and have only attracted attention in recent years. For example, Aydogan et al., based on long-term field warming experiments on grassland (mainly Arrhenatherum elatius and Galium album ), increased the surface temperature by 2 °C and found that warming did not affect the total colonization and concentration of leaf-associated bacterial cells, But it alters the diversity and phylogenetic composition of bacterial communities. More importantly, climate warming has led to the reduction of beneficial bacteria (such as Sphingomona s spp. and Rhizobium spp.) in grassland ecosystems , and potential pathogenic bacteria (such as Enterobacteriaceae , Pseudomonas spp. Pseudomonas and Acinetobacter ), which may indicate that climate warming increases the potential spread of pathogenic bacteria in grassland ecosystems. In addition to affecting foliar bacterial communities, climate warming also reduced the) and the richness and evenness of fungal communities in boreal forest trees and altered the overall composition of fungal communities. Warming negatively affected putative fungal pathogens compared with potential bacterial pathogens such as Acinetobacter. These excellent studies provide valuable information on the effects of climate warming on phyllosphere microbial community profiles. However, caution must be exercised in interpreting the results of each study as only a limited number of plant species and genotypes were considered. Differences in leaf traits, nutrient composition, and primary/secondary metabolites across genotypes may lead to differences in microbial colonization, which may mask the effects of climate warming. For example, studies have shown that long-term warming had no significant effect on the phyllosphere fungal community composition of three perennial herbs ( Achnatherum lettermanii , Festuca thurberi , and Poa pratensis ). Therefore, although some excellent research work has been done in this area, it is unclear whether the response of plant phyllosphere microbial communities to climate warming is consistent across species and genotypes . In addition, current research on phyllosphere microbial communities mainly focuses on bacterial and fungal communities, while other microbes such as archaea and protists are less studied. All of these findings underscore the need to improve our understanding of the warming phyllosphere microbial community.
Fig. 3 Influencing factors of phyllosphere microbial community. The phyllosphere consists of the above-ground parts of the plant, with different microorganisms in both the epiphytic and endophytic niches of the plant. These microbiota are acquired through vertical transmission through parental inheritance and horizontal transmission through the surrounding environment such as soil and air. On the one hand, global changes such as climate warming, drought and precipitation may affect leaf functional traits and phyllosphere microbial community characteristics, the latter mediating hydraulic activation of leaf water uptake (FWU)-related stomata. On the other hand, chemical fertilization can also affect the phyllosphere microbial community by altering the rhizosphere community and leaf morphology.
7 Effects of precipitation and drought on phyllosphere microbial communities
Under global climate change, precipitation begins to show a long-term downward trend, resulting in an increase in the frequency and duration of global droughts. At the same time, extreme weather events such as floods and droughts have been recorded more sharply and frequently. This global-scale change is expected to have a major impact on global agricultural production, as it can affect plant growth and the occurrence of plant diseases by altering humidity and water availability. According to a recent large-scale survey showing that precipitation is the most important predictor of fungal communities and abundance of phytopathogenic fungi, the abundance of phytopathogenic fungi could increase 100-fold by 2050, especially in coastal areas . Interactions between water status, soil fertility, and arbuscular mycorrhizal fungi can also affect phyllosphere microbial communities, for example, both water status and mycorrhizal disruption can reduce phyllosphere bacterial richness and bacterial community composition in tomato ( Solanum lycopersicum ) Evenness. In addition, high humidity can transform the non-pathogenic bacterium Pseudomonas syringae into a strong pathogenic bacterium, and induce the homeostasis of the symbiotic flora by affecting the water state in the chloroplast. Furthermore, drought stress not only affects the composition of phyllosphere microorganisms, but also affects the assembly process of the community . A recent systematic mass sampling study of sorghum showed that under drought stress, the assembly of the phyllosphere microbiota is determined by stochastic processes such as drift or random dispersal during the early stages of host development. For precipitation, in recent years, the wetland plant Typha latifolia) showed that rainfall events did not significantly affect the phyllosphere bacterial community richness and evenness. In contrast, climatic and leaf-related variables effectively shaped the seasonal dynamics of foliar microbial diversity and composition. Improving our understanding of how plant species and their microbial communities respond to drought events in the context of climate change is one of the most relevant topics in plant science. Leaf water uptake (FWU) has been identified as a mechanism commonly employed by trees and other plants in various biomes to predict the susceptibility of plant species to drought. In addition to morphological anatomical characteristics and leaf age, leaf wettability also depends on the coverage of phyllosphere microorganisms (epiphytes and endophytes), which affects its hydrophobicity. For example, biosurfactants produced by epiphyte bacteria may increase the permeability of the epidermis and allow water to diffuse through the epidermis, suggesting their potential effect on FWU. In addition, the phyllosphere microbial community can also mediate the hydraulic activation of stomata, which is related to the FWU pathway. For example, fungi can increase stomatal conductance, while bacteria can regulate stomata closing and opening. Stomata are the gates for plant pathogens to enter plants, and the regulation of stomata by phyllosphere microbial communities is also a mechanism of plant defense. These findings suggest that phyllosphere microbial communities have great potential to improve plant drought resistance .
8 Eco-evolutionary dynamics of phyllosphere and its microbial community under global climate change
The eco-evolutionary dynamics of plant-microbe symbiotic systems have received increasing attention. Unfortunately, little research has been done in this area. In the current study, the impact of plant evolutionary history and contemporary evolution on the response of plants, soil and rhizosphere microorganisms to climate change has received much attention.
As a product of past evolutionary history, phylogenetic relationships among plant species can interact with climate change to alter plant microbial communities . The results showed that under non-drought conditions, the microbial community composition in the rhizosphere of cereals was influenced by phylogeny. The influence of host evolutionary history on microbial communities has been widely observed in plants, especially those of agricultural interest. However, drought increased the abundance of Actinobacteria, weakening the importance of host evolutionary history for microbial community structure. Furthermore, on contemporary timescales, both microbial communities and plant evolution can mediate plant-microbial community responses to climate change. Microbes typically have large population sizes and high genetic variability, which translates into powerful evolutionary dynamics that affect ecological processes. For example, Batstone et al. used a synthetic community approach to show that the nodule-forming bacterium Ensifer meliloti evolved rapidly and promoted a mutually beneficial symbiosis between the bacterium and its plant host, Medicago truncatula . Unlike microorganisms, there are more obstacles to plant evolution. However, evidence has emerged in recent years that plants have the potential to evolve rapidly. An experiment by terHorst et al. found adaptive changes in canola populations after three generations of drought treatment. When transplanted into common gardens in a humid environment, drought-adapted and drought-unadapted rape populations showed different soil microbiota shaping abilities.
We recognize that most existing studies focus on the eco-evolutionary dynamics between plants and soil/rhizosphere microbial communities, rather than microbial communities in other plant compartments including the phyllosphere . In addition, some evolutionary processes specific to plants (such as intraspecific and cross-species hybridization and the emergence of polyploid plants) that can introduce new genetic variation into wild plant populations have received little attention. Recent advances in ecological evolutionary dynamics have provided a new model system for the study of the role of plant evolution in ecological processes. For example, there is growing interest in using aquatic floating plants of the Lemnaceae family (commonly known as duckweed) to study the ecological and evolutionary responses of plants to environmental changes. Duckweed has high intraspecific genotypic and phenotypic diversity, and changes in species composition (ecological dynamics) and genotypic composition (evolutionary dynamics) during plant-microbe interactions can be observed on the same time scale. The high tractability of these model systems can expand the scope of observational studies and provide additional mechanistic understanding of the importance of plant-microbe system evolution.
Conclusion and opinion
The foliar microbiota plays a crucial role in enhancing the ability of plants to pass through environmental filters. Currently, however, we predict that changes in the phyllosphere microbiota have a limited ability to affect ecosystem function in a changing environment. Some fundamental questions remain unresolved: (1) What are the mechanisms that support host-microbe interactions within and across plant hosts? (2) What are the major microbial taxa in the phyllosphere that control or modulate plant performance (eg, nutrient uptake, plant disease inhibition, or growth)? (3) Interactions of phyllosphere microbial communities with other plant microbial communities? (4) In a changing world, how can we control the foliar microbiota to improve plant health and performance? (5) How host and phyllosphere microbial communities will evolve in response to global change, and the impact of this ecological evolution on ecosystem function remains to be explored. Therefore, we believe that interdisciplinary research is needed to fundamentally understand the impact of global change on phyllosphere microbial communities and related ecosystem functions. To better understand the response mechanisms of "symbionts" (collections of plants and their microbial communities living in or around them) to global change, we need to shift our research focus from the level of community ecology to the level of ecosystem ecology . Under the conditions of global climate change, the complex interactions between plant phyllosphere microbiota and host adaptation, as well as the ecological functions of these microorganisms in plant nutrient uptake, growth and survival, need to be systematically studied.
Citation : Yong-Guan Zhu, Chao Xiong, Zhong Wei, Qing-Lin Chen, Bin Ma, Shu-Yi-Dan Zhou, et al. 2021. Impacts of global change on the phyllosphere microbiome. New Phytologist n/a: https: //doi.org/https://doi.org/10.1111/nph.17928
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