The Coevolution of Plants and Microbes Underpins Sustainable Agriculture

Terrestrial plants evolution occurred in the presence of microbes, the phytomicrobiome. The rhizosphere microbial community is the most abundant and diverse subset of the phytomicrobiome and can include both beneficial and parasitic/pathogenic microbes. Prokaryotes of the phytomicrobiome have evolve...

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Main Authors: Dongmei Lyu, Levini A. Msimbira, Mahtab Nazari, Mohammed Antar, Antoine Pagé, Ateeq Shah, Nadia Monjezi, Jonathan Zajonc, Cailun A. S. Tanney, Rachel Backer, Donald L. Smith
Format: Article
Language:English
Published: MDPI AG 2021-05-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/9/5/1036
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author Dongmei Lyu
Levini A. Msimbira
Mahtab Nazari
Mohammed Antar
Antoine Pagé
Ateeq Shah
Nadia Monjezi
Jonathan Zajonc
Cailun A. S. Tanney
Rachel Backer
Donald L. Smith
author_facet Dongmei Lyu
Levini A. Msimbira
Mahtab Nazari
Mohammed Antar
Antoine Pagé
Ateeq Shah
Nadia Monjezi
Jonathan Zajonc
Cailun A. S. Tanney
Rachel Backer
Donald L. Smith
author_sort Dongmei Lyu
collection DOAJ
description Terrestrial plants evolution occurred in the presence of microbes, the phytomicrobiome. The rhizosphere microbial community is the most abundant and diverse subset of the phytomicrobiome and can include both beneficial and parasitic/pathogenic microbes. Prokaryotes of the phytomicrobiome have evolved relationships with plants that range from non-dependent interactions to dependent endosymbionts. The most extreme endosymbiotic examples are the chloroplasts and mitochondria, which have become organelles and integral parts of the plant, leading to some similarity in DNA sequence between plant tissues and cyanobacteria, the prokaryotic symbiont of ancestral plants. Microbes were associated with the precursors of land plants, green algae, and helped algae transition from aquatic to terrestrial environments. In the terrestrial setting the phytomicrobiome contributes to plant growth and development by (1) establishing symbiotic relationships between plant growth-promoting microbes, including rhizobacteria and mycorrhizal fungi, (2) conferring biotic stress resistance by producing antibiotic compounds, and (3) secreting microbe-to-plant signal compounds, such as phytohormones or their analogues, that regulate aspects of plant physiology, including stress resistance. As plants have evolved, they recruited microbes to assist in the adaptation to available growing environments. Microbes serve themselves by promoting plant growth, which in turn provides microbes with nutrition (root exudates, a source of reduced carbon) and a desirable habitat (the rhizosphere or within plant tissues). The outcome of this coevolution is the diverse and metabolically rich microbial community that now exists in the rhizosphere of terrestrial plants. The holobiont, the unit made up of the phytomicrobiome and the plant host, results from this wide range of coevolved relationships. We are just beginning to appreciate the many ways in which this complex and subtle coevolution acts in agricultural systems.
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spelling doaj.art-a40f3774867d4c50b49cf32c17d565fc2023-11-21T19:17:03ZengMDPI AGMicroorganisms2076-26072021-05-0195103610.3390/microorganisms9051036The Coevolution of Plants and Microbes Underpins Sustainable AgricultureDongmei Lyu0Levini A. Msimbira1Mahtab Nazari2Mohammed Antar3Antoine Pagé4Ateeq Shah5Nadia Monjezi6Jonathan Zajonc7Cailun A. S. Tanney8Rachel Backer9Donald L. Smith10Department of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaDepartment of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaDepartment of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaDepartment of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaDepartment of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaDepartment of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaDepartment of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaDepartment of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaDepartment of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaDepartment of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaDepartment of Plant Science, Macdonald Campus, McGill University, Montreal, QC H9X 3V9, CanadaTerrestrial plants evolution occurred in the presence of microbes, the phytomicrobiome. The rhizosphere microbial community is the most abundant and diverse subset of the phytomicrobiome and can include both beneficial and parasitic/pathogenic microbes. Prokaryotes of the phytomicrobiome have evolved relationships with plants that range from non-dependent interactions to dependent endosymbionts. The most extreme endosymbiotic examples are the chloroplasts and mitochondria, which have become organelles and integral parts of the plant, leading to some similarity in DNA sequence between plant tissues and cyanobacteria, the prokaryotic symbiont of ancestral plants. Microbes were associated with the precursors of land plants, green algae, and helped algae transition from aquatic to terrestrial environments. In the terrestrial setting the phytomicrobiome contributes to plant growth and development by (1) establishing symbiotic relationships between plant growth-promoting microbes, including rhizobacteria and mycorrhizal fungi, (2) conferring biotic stress resistance by producing antibiotic compounds, and (3) secreting microbe-to-plant signal compounds, such as phytohormones or their analogues, that regulate aspects of plant physiology, including stress resistance. As plants have evolved, they recruited microbes to assist in the adaptation to available growing environments. Microbes serve themselves by promoting plant growth, which in turn provides microbes with nutrition (root exudates, a source of reduced carbon) and a desirable habitat (the rhizosphere or within plant tissues). The outcome of this coevolution is the diverse and metabolically rich microbial community that now exists in the rhizosphere of terrestrial plants. The holobiont, the unit made up of the phytomicrobiome and the plant host, results from this wide range of coevolved relationships. We are just beginning to appreciate the many ways in which this complex and subtle coevolution acts in agricultural systems.https://www.mdpi.com/2076-2607/9/5/1036plant evolutionphytomicrobiomesymbiosispathogenic interactionholobiont
spellingShingle Dongmei Lyu
Levini A. Msimbira
Mahtab Nazari
Mohammed Antar
Antoine Pagé
Ateeq Shah
Nadia Monjezi
Jonathan Zajonc
Cailun A. S. Tanney
Rachel Backer
Donald L. Smith
The Coevolution of Plants and Microbes Underpins Sustainable Agriculture
Microorganisms
plant evolution
phytomicrobiome
symbiosis
pathogenic interaction
holobiont
title The Coevolution of Plants and Microbes Underpins Sustainable Agriculture
title_full The Coevolution of Plants and Microbes Underpins Sustainable Agriculture
title_fullStr The Coevolution of Plants and Microbes Underpins Sustainable Agriculture
title_full_unstemmed The Coevolution of Plants and Microbes Underpins Sustainable Agriculture
title_short The Coevolution of Plants and Microbes Underpins Sustainable Agriculture
title_sort coevolution of plants and microbes underpins sustainable agriculture
topic plant evolution
phytomicrobiome
symbiosis
pathogenic interaction
holobiont
url https://www.mdpi.com/2076-2607/9/5/1036
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