Author's note: Starlight does not ask passers-by, and time pays off those who do it. It has been nearly 6 years since I entered the field of soil microbiology. The smooth development of this work is inseparable from the accumulation and precipitation of the author's team in this field, and is also closely related to the nutrition the author has drawn from the relevant official account. Recalling the past, when I participated in the first offline training organized by the Macro Genomics official account, I can vividly remember the scene where all the trainers gave each other their money. It can be said that the teachers of the metagenomics public account are the guides who led me into the door of soil multi-omics analysis. The server construction, multi-omics process construction, and data analysis visualization involved in the research all benefited from the high-quality training provided by metagenomics. Talking about the present, since then, I have learned a lot of explanations of esoteric ecological theories and data cleaning, analysis and visualization skills from public accounts such as Listenlii, Little White Fish's Life Notes, Holobionts, Red Queen Academic, Microbiology, VisualHub, etc. . I sincerely thank friends who are familiar with me and friends who are unfamiliar with me for providing a lot of dry goods! Looking forward to the future, we are willing to work together with you to decipher the mystery of China's soil microbiome and demonstrate the power of China's soil science to the international academic community.
Plant domestication shapes wheat rhizosphere microbiome assembly and metabolic function
Plant domestication shapes rhizosphere microbiome assembly and metabolic functions
Article，2023-03-31，Microbiome，[IF 16.837]
DOI：https://doi.org/10.1186/s40168-023-01513-1
Original link : https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-023-01513-1
First Authors: Hong Yue (肖红); Wenjie Yue (邓文杰)
Corresponding Authors: Duntao Shu (Shu Duntao); Weining Song (Song Weining); Gehong Wei (Wei Gehong)
Co-authors: Shuo Jiao (Jiao Shuo); Hyun Kim; Yong-Hwan Lee
Main unit:
Northwest A&F University (State Key Laboratory of Crop Stress Biology in Arid Areas, College of Life Sciences, College of Agronomy, Northwest A&F University, Yangling, Xianyang, 712100, Shaanxi, China)
Seoul National University (Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea)
- Summary -
The rhizosphere microbiome is influenced by host genotype, root exudates, and plant acclimatization processes, and is critical for the entire growth stage of plants. How the wheat domestication process shapes specific rhizosphere microbiomes and metabolic functions, and how the specific root exudates formed during the domestication process target the recruitment of core microorganisms is still unclear. In this study, the authors explored the ecological roles of specific rhizosphere microbiomes of tetraploid wild and domesticated wheat and their root exudates in recruiting rhizosphere microbiome functions through joint multi-omics analysis. The results showed that the plant rhizosphere microbiome is jointly determined by the host genotype and the domestication state, and plant domestication profoundly affects the assembly and metabolic function of the rhizosphere microbiome. Domestication destabilized the microbial network and reduced the abundance of key fungal communities, shifting the dominant species of the rhizosphere microbial community from fungi to carbon-fixing bacteria. Domestication reshaped the metabolic functions of rhizosphere microorganisms. The rhizosphere microorganisms of wild tetraploid wheat had the functions of nitrification, denitrification and phosphorus mineralization, while the rhizosphere microorganisms of cultivated tetraploid wheat had the functions of nitrogen fixation, ammonification and so on. And inorganic phosphorus dissolution and other functions. Domestication recruits bacterial and fungal communities with different substrate preferences. Host plants are able to recruit key microorganisms with special functions by releasing root exudates, thereby maintaining multi-nutrient cycling and plant health in farmland soil. This study clarified the key role of crop domestication in shaping the structure and function of the rhizosphere microbiome, providing scientific guidance for the sustainable development of food production.
- Introduction -
Plant domestication is a complex evolutionary process and an important achievement in human history. It provides a constant food supply, enhances the establishment of stable human settlements, and has a profound impact on human prosperity. The earliest crop plants were domesticated about 13,000 years ago, and a large number of crops, such as rice, wheat, and barley, have been domesticated through human intervention in modern agricultural areas. Improvements in phenotypic characteristics of domesticated cultivars are determined not only by their own genetic characteristics but also by their root-associated microbial communities. Previous studies have shown that plant domestication profoundly affects the assembly of seed and root microbiomes, especially the rhizosphere microbiome. These affected rhizosphere microbiomes have important roles in crop growth. Therefore, dissecting the species coexistence mechanisms of these affected microbiomes and the plant-microbiome interactions at the root-soil interface will provide new avenues for harnessing native rhizosphere microbiota to promote soil health and crop production.
Domestication of wild tetraploid wheat in the Fertile Crescent about 10,000 years ago was critical to human prosperity but also altered wheat genetic diversity. Understanding the differences in root microbial community assembly and function resulting from wheat domestication will provide a theoretical basis for maintaining soil health and precisely constructing wheat breeding strategies. The research aims to reveal the cross-border interaction and adaptive strategies of rhizosphere microorganisms during wheat domestication, decipher the functional characteristics and nutrient acquisition strategies of rhizosphere microbiomes, reveal the correlation between root exudates and aboveground plant phenotypes, and finally discover the key Effects of rhizosphere microbial taxa and single flora on wheat root morphological characteristics.
- result -
Domestication alters microbial communities and transboundary interaction network relationships
Domestication altered microbial taxonomic patterns and interkingdom co‑occurrences
Based on the genome-wide phylogenetic analysis of tetraploid wheat, 3 wild wheats and 3 domesticated wheats were selected ( Fig. 1 ), and the study found that the rhizosphere microbiome of wheat was jointly determined by the host genotype and domestication status. The rhizosphere microbiome was significantly affected by plant domestication status ( Fig. 2A and B ), and the wheat genome contributed more to the microbial diversity and composition of the rhizosphere bacterial community than the fungal community, while plant domestication status had a greater impact on the fungal community. Random forest analysis showed that bacteria were mainly from Proteobacteria, Bacteroidetes and Actinobacteria ( Fig. 2C ), and fungi were mainly from Ascomycota and Basidiomycota with higher community richness ( Fig. 2D ). At the same time, microbial collinear network analysis revealed that domestication destabilized the microbial network and reduced the abundance of key fungal communities, shifting the dominant species of the rhizosphere microbial community from fungi to bacteria (Fig. 3A and B ) .
Fig. 1 Global distribution and phenotypes of wild tetraploid wheat and domesticated wheat.
(A) and (B) Phylogenetic trees and geographical distribution of wild tetraploid wheat and domesticated wheat; (C) wheat plant height, thousand-grain weight, and seed aspect ratio.
Fig. 2 Differences in rhizosphere microbial communities between wild wheat and domesticated wheat.
The recruitment and consumption of bacteria (A) and fungi (B) in the rhizosphere of wild wheat compared with domesticated wheat; and the distribution characteristics of rhizosphere (C) and fungi (D), showing the top 20 ASVs in the community abundance .
Fig. 3 Correlation network and node topology characteristics among rhizosphere microorganisms.
Rhizosphere microbial transboundary network of domesticated wheat (A) and wild wheat (B); network node topology characteristics of domesticated wheat (C) and wild wheat (D).
Acclimatization status affects functional characteristics of the rhizosphere microbiome
Domestication status affects the functional profiles of the rhizosphere microbiome
Domestication has reshaped the key functions of rhizosphere microorganisms. The rhizosphere microorganisms of wild wheat have functions such as nitrification, denitrification and phosphorus mineralization, and mainly focus on translation, replication, repair and folding in genetic information processing pathways, sorting and degradation aspects. The rhizosphere microorganisms of domesticated wheat have the functions of inorganic nitrogen fixation, ammonification, and inorganic phosphorus dissolution, and are mainly enriched in the two-component system, fatty acid degradation, and quorum sensing pathways (Figure 4 ) .
Fig. 4 Functional characteristics of the rhizosphere microbiome of domesticated wheat and wild wheat
(A) KO functional categories and pathways; (B) distribution of functional genes related to different enriched pathways
Interactions between root exudates and microbial communities and crop phenotypes
Root metabolite traits and their links with the microbial community and plant phenotype profiles
By further mining the interrelationships between root exudates and microbiome and crop phenotypes, correlation analyzes revealed that domestication recruited bacterial and fungal communities with different substrate preferences (Fig. 5). Host plants are able to recruit key microorganisms with special functions by releasing root exudates, thereby maintaining multi-nutrient cycling and plant health in farmland soil. Microbial community inoculation experiments showed that the root length of inoculated wheat was inhibited and the average root diameter increased ( Fig. 6B ). We further found that M. mitrae significantly inhibited seedling and root growth in both wild and cultivated wheat ( Fig. 6C, D and E ).
Figure 5 Metabolic correlation analysis (MWAS) of rhizosphere bacteria and fungi enriched in domesticated and wild wheat
Fig. 6 Morphological characteristics of roots after rhizosphere microbial community inoculation.
(A) Schematic diagram of microbial community inoculation experiment; (B) Root length and average root diameter of domesticated wheat and wild wheat in the control and after inoculation; (C) Schematic diagram of M. mitrae inoculation; (D) Inoculation with M. mitrae and control The structural characteristics of the root system; (E) and (F) Morphological characteristics of the seedlings and roots after inoculation with M. mitrae and the control.
discuss
During the domestication of wheat, rhizosphere microbes were selectively recruited through the release of root exudates, thereby strongly affecting the rhizosphere microbial community structure, while leading to a decline in microbial gene diversity and a shift in functional traits, especially in relation to the cycling of multiple nutrients, For example, the abundance of carbon, nitrogen, and phosphorus cycle function genes decreased. Wheat domestication has important implications for soil biogeochemical processes, including carbon fixation, nitrate reduction, and organophosphate mineralization. Moreover, domestication reduces the stability of the microbial community. In domesticated wheat, bacteria play an important role, while in wild wheat, fungi play a more important ecological role. In addition, we found that root exudates specifically recruit rhizosphere microorganisms, Determine the morphological characteristics of the aboveground and underground parts ( Figure 7 ). This study greatly deepens our understanding of rhizosphere microbe-plant coexistence and functional adaptation during wheat domestication, and provides a scientific reference for new wheat breeding strategies.
Figure 7. Conceptual model of plant domestication shaping rhizosphere microbial community assembly and metabolic function.
references
Hong Yue, Wenjie Yue, Shuo Jiao, Hyun Kim, Yong-Hwan Lee, Gehong Wei, Weining Song, Duntao Shu. ( 2023 ) . Plant domestication shapes rhizosphere microbiome assembly and metabolic functions. Microbiome . doi: 10.1186/s40168 01513-1.
- About the Author -
First author
NWAFU
Yue Hong
lecturer
Yue Hong is a lecturer at the College of Agriculture, Northwest A&F University. She mainly focuses on the interaction between plants and rhizosphere microorganisms, the mining of wheat stress-resistant germplasm resources, and the mining of functional genes. Currently as the first author, he has published related papers on Microbiome, Plant Biotechnology Journal, IJMS and Science of the Total Environment.
Zhejiang University
Yue Wenjie
postdoctoral fellow
Currently working as a postdoctoral researcher at the School of Agriculture and Biotechnology, Zhejiang University, focusing on plant genome evolution, horizontal gene transfer, gene expression regulation, plant stress molecular biology and population genetics. At present, 5 SCI papers have been published in journals such as Microbiome, International journal of molecular sciences, Journal of plant physiology and Frontiers in plant science.
Corresponding Author
NWAFU
Wei Gehong
Professor, Doctoral Supervisor
Wei Gehong, professor and doctoral supervisor of the School of Life Sciences, Northwest A&F University. "Cheung Kong Scholars" Distinguished Professor, winner of the National Science Fund for Distinguished Young Scholars and National 100 Outstanding Doctoral Dissertations, leading talent in scientific and technological innovation of the Ten Thousand Talents Program, and chief expert of the National "863" Program. Long-term commitment to the diversity and utilization of soil microbial resources, rhizosphere microorganisms and soil fertility improvement and other basic theory and key technology research. He has published more than 100 academic papers in ISME J, Microbiome, Global Change Biology, Soil Biology and Biochemistry, Environmental Science & Technology and other internationally renowned journals in this field. Deputy director of the professional committee, deputy director of the Soil Biology and Biochemistry Professional Committee of the Soil Society of China.
NWAFU
Song Weining
Professor, Doctoral Supervisor
Song Weining, professor and doctoral supervisor of the School of Agriculture, Northwest A&F University. Received a Ph.D. in Wheat Genomics from the University of Adelaide in 1994. From 1992 to 1997, he served as a molecular biologist at the Queensland Agricultural Biotechnology Center and the Plant Genetic Resources Conservation Center of Southern Cross University. Head of the Molecular Biology Laboratory of the Research Center. From 2002 to 2006, he served as a senior researcher at the Institute of Evolution, Haifa University, Israel. In February 2006, he returned to work full-time at the Agricultural College of Northwest A&F University. Mainly engaged in wheat molecular biology, genomics and genetic improvement, plant stress genomics and plant origin and domestication research. Published more than 40 teaching and research papers.
NWAFU
Shu Duntao
Associate Professor
Shu Duntao, associate professor, College of Life Sciences, Northwest A&F University. Committed to the study of environmental nitrogen cycle process. I was immersed in the research of anammox technology. After graduating from a Ph.D., he transferred from the field of environmental engineering to soil science, focusing on the process of soil nitrogen cycle and soil health in arid areas. In the past five years, as the first or corresponding author, he has published many related papers in internationally renowned journals such as Microbiome, Science of The Total Environment, Bioresource Technology, Chemical Engineering Journal, Applied Soil Ecology, etc. Presided over the National Natural Science Foundation of China projects, national key research and development sub-projects, young scientists sub-projects, etc. Sincerely welcome students related to environmental microbiology, ecology, and soil science to apply for the postgraduates of the above-mentioned teams. Maybe the joint research results of you and me can appear in high-level journals together again.
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