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# Impact of global change on the plant microbiome

Stéphane Hacquard, Ertao Wang, Holly Slater, Francis Martin

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Stéphane Hacquard, Ertao Wang, Holly Slater, Francis Martin. Impact of global change on the plant microbiome. New Phytologist, 2022, 234 (6), pp.1907-1909. 10.1111/nph.18187. hal-04001861

HAL Id: hal-04001861

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Submitted on 23 Feb 2023

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Editorial

Impact of global change on the
plant microbiome

Plant-associated microorganisms may be invisible to the naked
eye, yet they play a key role in the future sustainability of
terrestrial ecosystems – from arable lands to rainforests, through
tundra and taiga to deserts. It is now widely recognized that
climate change dramatically impacts plant performance and
physiology. However, plants are not living alone, they are supra-
organisms hosting a wide range of commensal, beneficial and
detrimental microbes. The plant with its associated microbiota –
the collection of all microorganisms in a location – faces altered
environmental conditions as a result of a rapidly changing
climate. The signs of climate change are undeniable, and the
dramatic impact for plant and microbial inhabitants of our
planet is a serious concern. Warming strikingly shifts both the
phylogenetic and functional structures of soil microbial com-
munities, which lead to unknown alterations in communities and
processes. Similarly, plants and their microbial consortium are
directly impacted by changing environmental conditions leading
to different plant interaction characteristics, altered ecology, as
well as a change in functioning. Most importantly, the plant
microbiota might respond to changes in plant physiology, which
could affect the microbial diversity and functioning in a poorly
known, but critical, feedback loop. Microorganisms might also
play an important role for the plant in regard to adaptation to
changing conditions. Describing, understanding and predicting
the impacts of anthropogenically-driven climate change on
plant–microbe interactions and ecosystem functioning is there-
fore a scientific and societal challenge.

In this *New Phytologist* Special Issue dedicated to the plant
microbiota, several experts in the field discuss the microbial
contributions to climate change. In so doing they consider the
effects of global warming, extreme weather, flooding and other
consequences of climate change on microbial communities in
terrestrial ecosystems and on host–microbiota interactions. They
explore open questions and research needs including: *How do global
environmental changes affect the phylogenetic diversity and physiology
of the plant-associated microorganisms in the environment? What are
the consequences of this change on plant biology and development? How
can the effects of global change on microbial communities be mitigated?
How can we deal with both the spatial and temporal scales of research
questions arising in global change microbiology? What are the current
open questions, research needs and priorities?* As a follow-up, this
collection of papers describe how climate change affects plant–
microbe associations, which mechanisms are involved, and what
effects on ecosystem function can be expected in the long term. The
authors explore the plant-associated microbiota world across all

scales from the genomic to ecosystem level, including above- and
below-ground interactions. They address the effects of global
environmental changes on the diversity, functioning and evolution
of the plant microbiota and how these changes are altering different
types of interactions, including symbiotic and endophytic associ-
ations, as well as multi-partite interactions. Several studies also
investigated how beneficial microorganisms play a role in plant
adaptation to stress conditions.

The overarching objective of this collection is to provide a
platform for discussion of the most pressing issues influencing
microbial communities and their interactions with their host plant
and then, to integrate information from different approaches. With
this in mind, we aim to create a systematic framework to
understand and improve plant–microbe interactions under typical
stress conditions (e.g. increase of CO2, drought, soil warming,
salinity), related to global environmental changes. Of note, the
articles in this Special Issue discuss the interactions of plants with a
wide range of microbes, including bacteria or fungi, beneficial
microbes or pathogens and cover molecular approaches to
ecosystems implications. Through this collection we hope to
obtain and further stimulate a systematic understanding and
interest in the interaction between plants, beneficial microorgan-
isms, pathogens and environment.

According to the different original research articles, global
change factors are expected to have profound impacts not only
on the composition, but also on the function of the plant
microbiota. These effects can induce changes in the microbiota
either directly, or indirectly via global change-induced modula-
tion of the host and/or the environment (Fig. 1a). In particular,
drought was found to alter the composition and diversity of
arbuscular mycorrhizal (AM) fungal communities (Fu et al.,
2022, in this issue pp. 2003–2017), to induce shifts in
aboveground microbial assemblages (Debray et al., 2022, in this
issue pp. 2018–2031) and to trigger transcriptional acclimation
in the etomycorrhizal fungus *Suillus pungens* (Erlandson et al.,
2022, in this issue pp. 1910–1913). In addition to water deficits,
warming was reported to modulate turnover of mycorrhizal
fungal mycelium in peatland via shifts in microbial decomposer
assemblages (Maillard et al., 2022, in this issue pp. 2032–2043)
and is predicted to alter the assembly of nitrogen fixing taxa in
sub-Arctic tundra (Klarenberg et al., 2022, in this issue pp.
2044–2056) (Fig. 1b). These data, together with the observation
that (1) high nitrogen fertilisation can disrupt normal temporal
dynamics of AM fungal communities in an agricultural field
(Babalola et al., 2022, in this issue pp. 2057–2072), and (2)
replacement of native birch by fast growing spruce extensively
modulate soil bacterial and fungal assemblages in boreal forests
(Mundra et al., 2022, in this issue pp. 2073–2087), illustrate the
invisible, yet major, impacts that anthropogenically-driven
perturbations have on belowground microbial populations
(Fig. 1b). Whether these global change-induced perturbations
in belowground microbial populations will have major
consequences on plant health, plant distribution, and plant
adaptation to stress remains a key unanswered question.

Given that microbes have interacted with their host plants for
450 million years combined with reports of evidence for co-
evolution (i.e. Abdelfattah et al., 2022, in this issue pp. 2088–
2100), it becomes clear that numerous microbial functions have
been co-opted by plants to promote adaptation to environmental
constraints. Therefore, the potential to use the plant microbiome to
promote host tolerance to global change stressors is high (Fig. 1b).
Different strategies have been discussed here, including: (1)
iterative root microbiome selection to alleviate salt stress (King
et al., 2022, in this issue pp. 2101–2110); (2) use of habitat-adapted
microbiomes to promote host tolerance to warming (Carrell et al.,
2022, in this issue pp. 2111–2125); and (3) utilization of microbes
from extreme desert environments (Maldonado et al., 2022, in this
issue pp. 2126–2139). Particularly, the observation that habitat-
adapted microbial communities can transmit thermotolerance to
*Sphagnum* peatmoss and can promote resilience to warming

demonstrates that rapid adaptation to stress in the host can occur
via the microbiota (Carrell *et al.*, 2022). Taken together, the results
suggest that microbial commensals and symbionts might represent
key components promoting host survival and rapid adaptation to
environmental perturbations.

This collection also includes a number of Tansley reviews and Tansley insights, Research reviews and Viewpoints that discuss various aspects including the role of beneficial fungi for promoting stress tolerance (Almario et al., 2022, in this issue pp. 1967–1976), the potential of root metabolome engineering for modulating beneficial plant–microbe interactions (Hong et al., 2022; in this issue pp. 1945–1950), the consequences of climate change on phyllosphere/rhizosphere microbiomes and mountain microbial biogeography (Zhu et al., 2022, pp. 1977–1986; Trivedi et al., 2022, pp. 1951–1959; Wang et al., 2022, pp. 1987–2002), as well as the consequences of introducing probiotic microbial taxa in ecosystems (Moore et al., 2022, in this issue pp. 1914–1918). The articles in the collection also stress the importance of considering host-specificity (Semchenko et al., 2022, in this issue pp. 1929–1944), eco-evolutionary aspects (Angulo et al., 2022, in this issue

<figure><img src="image_5.png" /><figcaption>**Fig. 1** A collection of articles to understand how global change factors affect plant–microbiota associations. (a) Direct and indirect effects of global change factors on the plant microbiota. Indirect effects occur via the host–environment–microbiota triangle. (b) Global change factors alter plant microbiota assemblages and modulate beneficial plant–microbe interactions. Plant adaptation to rapid environmental changes is expected to depend on plant–microbiota associations. The 20 articles of this *New Phytologist* Special Issue are highlighted according to the respective themes. Reviews and Viewpoints are indicated by an asterisk.</figcaption></figure>
pp. 1919–1928), and belowground–aboveground diversity link-
ages (Fei *et al.*, 2022, in this issue pp. 1960–1966) to understand
how microbes affect plant ecological responses to global change.

We hope that this collection of papers will result in a better
understanding on how microbial colonization and assemblages,
plant-pathogen and plant-beneficial microorganism interactions
are affected in altered climate conditions. Additional knowledge
should be obtained on the follow-up effects on ecosystem function-
ing and to what extent beneficial microorganisms may alleviate stress
conditions due to climate change. This will rely on developing
interdisciplinary research projects that aim to understand how
microbial activities and metabolic fluxes alter as climate, precipita-
tion, and temperatures change globally. Shedding light on these
questions should include ‘genes-to-ecosystems’ approaches. The
studies presented here are intended to highlight and further stimulate
research on the functioning and role of the plant microbiota, and its
interaction with plants under stress. Defining the components,
dynamics, functions and interactions of the core plant-associated
microbiota will assist in developing microbiome-based solutions to
create healthy, resilient and sustainable plant ecosystems.

ORCID

Stéphane Hacquard ID https://orcid.org/0000-0003-2293-3525

Francis Martin https://orcid.org/0000-0002-4737-3715

Holly Slater https://orcid.org/0000-0002-3477-9767

Ertao Wang https://orcid.org/0000-0002-5178-3530

Stéphane Hacquard¹ ID , Ertao Wang² ID , Holly Slater³ ID
and Francis Martin⁴* ID

¹Max Planck Institute for Plant Breeding Research,
50829 Cologne, Germany;

²National Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China;

³New Phytologist Central Office, Lancaster University,
Bailrigg House, Lancaster, LA1 4YE, UK;

⁴Institut national de recherche pour l'agriculture, l'alimentation et l'environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy, Université de Lorraine, 54280 Champenoux, France

(*Author for correspondence: email francis.martin@inrae.fr)

References

Abdelfattah A, Tack AJM, Wasserman B, Liu J, Berg G, Norelli J, Droby S,  
Wisniewski M. 2022. Evidence for host–microbiome co-evolution in apple. *New  
Phytologist* 234: 2088–2100.

Almario J, Fabiańska I, Saridis G, Bucher M. 2022. Unearthing the plant–microbe *quid pro quo* in root associations with beneficial fungi. *New Phytologist* 234: 1967–1976.

Angulo V, Beriot N, Garcia-Hernandez E, Li E, Masteling R, Lau JA. 2022. Plant-microbe eco-evolutionary dynamics in a changing world. *New Phytologist* 234: 1919–1928.

Babalola BJ, Li J, Willing CE, Zheng Y, Wang Y-L, Gan H-Y, Li X-C, Wang C, Adams CA, Gao C *et al*. 2022. Nitrogen fertilisation disrupts the temporal dynamics of arbuscular mycorrhizal fungal hyphae but not spore density and community composition in a wheat field. *New Phytologist* 234: 2057–2072.

Carrell AA, Lawrence TJ, Cabugao KGM, Carper DL, Pelletier DA, Lee JH, Jawdy SS, Grimwood J, Schmutz J, Hanson PJ *et al*. 2022. Habitat-adapted microbial communities mediate *Sphagnum* peatmoss resilience to warming. *New Phytologist* 234: 2111–2125.

Debray R, Socolar Y, Kaulbach G, Guzman A, Hernandez CA, Curley R, Dhond A, Bowles T, Koskella B. 2022. Water stress and disruption of mycorrhizas induce parallel shifts in phyllosphere microbiome composition. *New Phytologist* 234: 2018–2031.

Erlandson SR, Margis R, Ramirez A, Nguyen N, Lofgren LA, Liao H-L, Vilgalys R, Kennedy PG, Peay KG. 2022. Transcriptional acclimation and spatial differentiation characterize drought response by the ectomycorrhizal fungus *Suillus pungens*. *New Phytologist* 234: 1910–1913.

Fei S, Kivlin SN, Domke GM, Jo I, LaRue EA, Phillips RP. 2022. Coupling of plant and mycorrhizal fungal diversity: its occurrence, relevance, and possible implications under global change. *New Phytologist* 234: 1960–1966.

Fu W, Chen B, Rillig MC, Jansa J, Ma W, Xu C, Luo W, Wu H, Hao Z, Wu H *et al.* 2022. Community response of arbuscular mycorrhizal fungi to extreme drought in a cold-temperate grassland. *New Phytologist* 234: 2003–2017.

Hong Y, Zhou Q, Hao Y, Huang AC. 2022. Crafting the plant root metabolome for improved microbe-assisted stress resilience. *New Phytologist* 234: 1945–1950.

King WL, Kaminsky LM, Gannett M, Thompson GL, Kao-Kniffin J, Bell TH. 2022. Soil salinization accelerates microbiome stabilization in iterative selections for plant performance. *New Phytologist* 234: 2101–2110.

Klarenberg IJ, Keuschnig C, Russi Colmenares AJ, Warshan D, Jungblut AD, Jónsdóttir IS, Vilhelmsson O. 2022. Long-term warming effects on the microbiome and *nifH* gene abundance of a common moss species in sub-Arctic tundra. *New Phytologist* 234: 2044–2056.

Maillard F, Fernandez CW, Mundra S, Heckman KA, Kolka RK, Kauserud H, Kennedy PG. 2022. Warming drives a 'hummockification' of microbial communities associated with decomposing mycorrhizal fungal necromass in peatlands. *New Phytologist* 234: 2032–2043.

Maldonado JE, Gaete A, Mandakovic D, Aguado-Norese C, Aguilar M, Gutiérrez RA, González M. 2022. Partners to survive: Hoffmannseggia doellii root-associated microbiome at the Atacama Desert. *New Phytologist* 234: 2126–2139.

Moore JAM, Abraham PE, Michener JK, Muchero W, Cregger MA. 2022. Ecosystem consequences of introducing plant growth promoting rhizobacteria to managed systems and potential legacy effects. *New Phytologist* 234: 1914–1918.

Mundra S, Kauserud H, Økland T, Nordbakken J-F, Ransedokken Y, Kjønaas OJ. 2022. Shift in tree species changes the belowground biota of boreal forests. *New Phytologist* 234: 2073–2087.

Semchenko M, Barry KE, de Vries FT, Mommer L, Moora M, Maciá-Vicente JG. 2022. Deciphering the role of specialist and generalist plant–microbial interactions as drivers of plant–soil feedback. *New Phytologist* 234: 1929–1944.

Trivedi P, Batista BD, Bazany KE, Singh BK. 2022. Plant–microbiome interactions under a changing world: responses, consequences and perspectives. *New Phytologist* 234: 1951–1959.

Wang J, Hu A, Meng F, Zhao W, Yang Y, Soininen J, Shen J, Zhou J. 2022. Embracing mountain microbiome and ecosystem functions under global change. *New Phytologist* 234: 1987–2002.

Zhu Y-G, Xiong C, Wei Z, Chen Q-L, Ma B, Zhou S-Y-D, Tan J, Zhang L-M, Cui H-L, Duan G-L. 2022. Impacts of global change on the phyllosphere microbiome. *New Phytologist* 234: 1977–1986.

**Key words:** global change, microbiome, microbiota, phyllosphere, plant–microbe interactions, rhizosphere, supra-organisms, sustainable terrestrial ecosystems.