{"title":"在驯化中迷失:现代小麦抛弃了微生物盟友吗?","authors":"Martin Balcerowicz","doi":"10.1111/tpj.17137","DOIUrl":null,"url":null,"abstract":"<p>The domestication of wheat (<i>Triticum aestivum</i>), which began approximately 10 000 years ago in the Fertile Crescent, was a pivotal event in the first agricultural revolution. It marked the shift from a hunter–gatherer lifestyle to one of settlement and agriculture. A key milestone in this process was the domestication of wild emmer wheat, which gave rise to cultivated tetraploid durum wheat and represents an important stepping stone towards modern bread wheat, which emerged 1500–2000 years later and is the most widely grown type of wheat today (Haas et al., <span>2019</span>). Domestication brought about substantial changes in wheat's morphology and development, including altered flowering time, larger grains, increased yield, reduced seed dormancy and the elimination of seed shattering.</p><p>Changes brought about by domestication are not restricted to the crop but also affect organisms interacting with it. Microorganisms living on and within the plant, collectively referred to as the plant's microbiome, play a crucial role in plant fitness, influencing growth, resistance and resilience throughout the plant's life cycle. Roots are a major interface between plants and soil microbes, with many microbes living as endophytes within the roots or colonising the surrounding soil (rhizosphere). Host plants release exudates to attract beneficial rhizospheric and endophytic bacteria, and the composition of these exudates shapes the root microbiome (Hu et al., <span>2018</span>). While several studies found that domestication reduced the diversity of rhizospheric microbes (e.g. Pérez-Jaramillo et al., <span>2016</span>), little research has explored how domestication affected the diversity of endophytes.</p><p>Hong Yue, corresponding author of the highlighted study, originally worked on plant resistance genes during her PhD, but gradually shifted her research focus towards plant–microbe interactions. Using metagenomics and metabolomics, Yue demonstrated that wild wheat varieties harbour a higher functional diversity in their rhizosphere microbiome than do domesticated cultivars (Yue et al., <span>2023</span>). Building on this work, undergraduate student Lixin Deng, under Yue's supervision, investigated the effects of domestication on wheat's endophytic bacterial community. For their studies, Deng chose three wild emmer accessions and three domesticated elite cultivars from a germplasm collection assembled by principal investigator Weining Song. These accessions, which represent six distinct branches of the wheat phylogenetic tree, had been grown at the Caoxingzhuang Agricultural Ecosystem Experimental Station of Northwest A&F University for 8 years prior to Deng's study, suggesting that any differences detected can be attributed to genetic variation rather than differences in origin.</p><p>To determine the composition of the endophytic microbiomes, DNA was extracted from the roots of mature wheat plants grown in the same soil and bacterial taxa were identified by sequencing prokaryote-specific 16S rRNA genes. Principal component analysis (PCA) of the sequencing data clearly separated wild and domesticated wheat varieties. Alpha diversity indices, which describe the diversity in microbial species and their abundance, were significantly higher for the domesticated cultivars, suggesting that domestication has increased endophyte diversity. While 110 bacterial genera were detected in both groups, albeit with differences in abundance, only one genus, <i>Serratia</i>, was unique to wild varieties and none were exclusive to domesticated cultivars. <i>Serratia</i> is known to enhance plant growth, particularly under salt stress and nutrient deprivation (Kulkova et al., <span>2024</span>), and may be an important factor for wild wheat's stress resilience.</p><p>Based on significant pairwise correlations, the authors constructed bacterial interaction networks for both wheat groups (Figure 1a). Network connectivity (i.e., the number of co-occurrences) was higher for wild than domesticated wheat; domestication thus seems to have destabilised wheat's bacterial co-occurrence network. The analysis also identified several genera, including growth-promoting <i>Chryseobacterium</i>, <i>Massilia</i> and <i>Lechevalieria</i>, as keystone taxa that play central roles in these bacterial networks.</p><p>In parallel with their microbiome analysis, the authors generated metabolic profiles of root exudates from the six wheat varieties. Again, wild and domesticated wheat samples clustered separately in PCA, with eight and six metabolites found exclusively in wild and domesticated wheat, respectively. These findings indicate that domestication substantially altered root metabolism. The researchers integrated these metabolomics data with their microbiome data and detected significant correlations between keystone taxa and multiple metabolites. Among these, <span>l</span>-tyrosine stood out for its higher abundance in wild wheat roots and its strong correlation with the presence of <i>Chryseobacterium</i>. To explore this further, the team grew wheat plants in controlled conditions and exposed them to <i>Chryseobacterium</i>, <span>l</span>-tyrosine or a combination of both. While neither treatment altered shoot or root growth of domesticated wheat varieties, the combined exposure to <span>l</span>-tyrosine and <i>Chryseobacterium</i> reduced root elongation, but increased root fresh weight, of wild wheat (Figure 1b). Several <i>Chryseobacterium</i> species are known to promote plant growth by solubilising nutrients and producing plant hormones (Jung et al., <span>2023</span>). The observations by Deng et al. support the hypothesis that wild wheat recruits or stimulates <i>Chryseobacterium</i> by the release of <span>l</span>-tyrosine, and that this beneficial relationship was lost during domestication.</p><p>Reshaping the microbiome represents a promising strategy for improving crop yield and resilience. Understanding how crops interact with their microbiomes, and how these interactions have changed through domestication, represents an important step towards this goal. The findings by Deng et al. highlight the potential of wild wheats and their microbiomes as valuable resources for improving modern wheat varieties. Bacteria such as <i>Serratia</i> and <i>Chryseobacterium</i> represent exciting candidates in this context, but changes to wheat's genetic make-up may be required to fully unlock the microbes' potential. Yue hopes that their studies will eventually lead to the development of microbial agents that can be applied in large-scale agricultural settings to enhance crop production.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":"120 4","pages":"1261-1262"},"PeriodicalIF":6.2000,"publicationDate":"2024-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/tpj.17137","citationCount":"0","resultStr":"{\"title\":\"Lost in domestication: Has modern wheat left its microbial allies behind?\",\"authors\":\"Martin Balcerowicz\",\"doi\":\"10.1111/tpj.17137\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p>The domestication of wheat (<i>Triticum aestivum</i>), which began approximately 10 000 years ago in the Fertile Crescent, was a pivotal event in the first agricultural revolution. It marked the shift from a hunter–gatherer lifestyle to one of settlement and agriculture. A key milestone in this process was the domestication of wild emmer wheat, which gave rise to cultivated tetraploid durum wheat and represents an important stepping stone towards modern bread wheat, which emerged 1500–2000 years later and is the most widely grown type of wheat today (Haas et al., <span>2019</span>). Domestication brought about substantial changes in wheat's morphology and development, including altered flowering time, larger grains, increased yield, reduced seed dormancy and the elimination of seed shattering.</p><p>Changes brought about by domestication are not restricted to the crop but also affect organisms interacting with it. Microorganisms living on and within the plant, collectively referred to as the plant's microbiome, play a crucial role in plant fitness, influencing growth, resistance and resilience throughout the plant's life cycle. Roots are a major interface between plants and soil microbes, with many microbes living as endophytes within the roots or colonising the surrounding soil (rhizosphere). Host plants release exudates to attract beneficial rhizospheric and endophytic bacteria, and the composition of these exudates shapes the root microbiome (Hu et al., <span>2018</span>). While several studies found that domestication reduced the diversity of rhizospheric microbes (e.g. Pérez-Jaramillo et al., <span>2016</span>), little research has explored how domestication affected the diversity of endophytes.</p><p>Hong Yue, corresponding author of the highlighted study, originally worked on plant resistance genes during her PhD, but gradually shifted her research focus towards plant–microbe interactions. Using metagenomics and metabolomics, Yue demonstrated that wild wheat varieties harbour a higher functional diversity in their rhizosphere microbiome than do domesticated cultivars (Yue et al., <span>2023</span>). Building on this work, undergraduate student Lixin Deng, under Yue's supervision, investigated the effects of domestication on wheat's endophytic bacterial community. For their studies, Deng chose three wild emmer accessions and three domesticated elite cultivars from a germplasm collection assembled by principal investigator Weining Song. These accessions, which represent six distinct branches of the wheat phylogenetic tree, had been grown at the Caoxingzhuang Agricultural Ecosystem Experimental Station of Northwest A&F University for 8 years prior to Deng's study, suggesting that any differences detected can be attributed to genetic variation rather than differences in origin.</p><p>To determine the composition of the endophytic microbiomes, DNA was extracted from the roots of mature wheat plants grown in the same soil and bacterial taxa were identified by sequencing prokaryote-specific 16S rRNA genes. Principal component analysis (PCA) of the sequencing data clearly separated wild and domesticated wheat varieties. Alpha diversity indices, which describe the diversity in microbial species and their abundance, were significantly higher for the domesticated cultivars, suggesting that domestication has increased endophyte diversity. While 110 bacterial genera were detected in both groups, albeit with differences in abundance, only one genus, <i>Serratia</i>, was unique to wild varieties and none were exclusive to domesticated cultivars. <i>Serratia</i> is known to enhance plant growth, particularly under salt stress and nutrient deprivation (Kulkova et al., <span>2024</span>), and may be an important factor for wild wheat's stress resilience.</p><p>Based on significant pairwise correlations, the authors constructed bacterial interaction networks for both wheat groups (Figure 1a). Network connectivity (i.e., the number of co-occurrences) was higher for wild than domesticated wheat; domestication thus seems to have destabilised wheat's bacterial co-occurrence network. The analysis also identified several genera, including growth-promoting <i>Chryseobacterium</i>, <i>Massilia</i> and <i>Lechevalieria</i>, as keystone taxa that play central roles in these bacterial networks.</p><p>In parallel with their microbiome analysis, the authors generated metabolic profiles of root exudates from the six wheat varieties. Again, wild and domesticated wheat samples clustered separately in PCA, with eight and six metabolites found exclusively in wild and domesticated wheat, respectively. These findings indicate that domestication substantially altered root metabolism. The researchers integrated these metabolomics data with their microbiome data and detected significant correlations between keystone taxa and multiple metabolites. Among these, <span>l</span>-tyrosine stood out for its higher abundance in wild wheat roots and its strong correlation with the presence of <i>Chryseobacterium</i>. To explore this further, the team grew wheat plants in controlled conditions and exposed them to <i>Chryseobacterium</i>, <span>l</span>-tyrosine or a combination of both. While neither treatment altered shoot or root growth of domesticated wheat varieties, the combined exposure to <span>l</span>-tyrosine and <i>Chryseobacterium</i> reduced root elongation, but increased root fresh weight, of wild wheat (Figure 1b). Several <i>Chryseobacterium</i> species are known to promote plant growth by solubilising nutrients and producing plant hormones (Jung et al., <span>2023</span>). The observations by Deng et al. support the hypothesis that wild wheat recruits or stimulates <i>Chryseobacterium</i> by the release of <span>l</span>-tyrosine, and that this beneficial relationship was lost during domestication.</p><p>Reshaping the microbiome represents a promising strategy for improving crop yield and resilience. Understanding how crops interact with their microbiomes, and how these interactions have changed through domestication, represents an important step towards this goal. The findings by Deng et al. highlight the potential of wild wheats and their microbiomes as valuable resources for improving modern wheat varieties. Bacteria such as <i>Serratia</i> and <i>Chryseobacterium</i> represent exciting candidates in this context, but changes to wheat's genetic make-up may be required to fully unlock the microbes' potential. Yue hopes that their studies will eventually lead to the development of microbial agents that can be applied in large-scale agricultural settings to enhance crop production.</p>\",\"PeriodicalId\":233,\"journal\":{\"name\":\"The Plant Journal\",\"volume\":\"120 4\",\"pages\":\"1261-1262\"},\"PeriodicalIF\":6.2000,\"publicationDate\":\"2024-11-17\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://onlinelibrary.wiley.com/doi/epdf/10.1111/tpj.17137\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"The Plant Journal\",\"FirstCategoryId\":\"2\",\"ListUrlMain\":\"https://onlinelibrary.wiley.com/doi/10.1111/tpj.17137\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"PLANT SCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"The Plant Journal","FirstCategoryId":"2","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/tpj.17137","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
Lost in domestication: Has modern wheat left its microbial allies behind?
The domestication of wheat (Triticum aestivum), which began approximately 10 000 years ago in the Fertile Crescent, was a pivotal event in the first agricultural revolution. It marked the shift from a hunter–gatherer lifestyle to one of settlement and agriculture. A key milestone in this process was the domestication of wild emmer wheat, which gave rise to cultivated tetraploid durum wheat and represents an important stepping stone towards modern bread wheat, which emerged 1500–2000 years later and is the most widely grown type of wheat today (Haas et al., 2019). Domestication brought about substantial changes in wheat's morphology and development, including altered flowering time, larger grains, increased yield, reduced seed dormancy and the elimination of seed shattering.
Changes brought about by domestication are not restricted to the crop but also affect organisms interacting with it. Microorganisms living on and within the plant, collectively referred to as the plant's microbiome, play a crucial role in plant fitness, influencing growth, resistance and resilience throughout the plant's life cycle. Roots are a major interface between plants and soil microbes, with many microbes living as endophytes within the roots or colonising the surrounding soil (rhizosphere). Host plants release exudates to attract beneficial rhizospheric and endophytic bacteria, and the composition of these exudates shapes the root microbiome (Hu et al., 2018). While several studies found that domestication reduced the diversity of rhizospheric microbes (e.g. Pérez-Jaramillo et al., 2016), little research has explored how domestication affected the diversity of endophytes.
Hong Yue, corresponding author of the highlighted study, originally worked on plant resistance genes during her PhD, but gradually shifted her research focus towards plant–microbe interactions. Using metagenomics and metabolomics, Yue demonstrated that wild wheat varieties harbour a higher functional diversity in their rhizosphere microbiome than do domesticated cultivars (Yue et al., 2023). Building on this work, undergraduate student Lixin Deng, under Yue's supervision, investigated the effects of domestication on wheat's endophytic bacterial community. For their studies, Deng chose three wild emmer accessions and three domesticated elite cultivars from a germplasm collection assembled by principal investigator Weining Song. These accessions, which represent six distinct branches of the wheat phylogenetic tree, had been grown at the Caoxingzhuang Agricultural Ecosystem Experimental Station of Northwest A&F University for 8 years prior to Deng's study, suggesting that any differences detected can be attributed to genetic variation rather than differences in origin.
To determine the composition of the endophytic microbiomes, DNA was extracted from the roots of mature wheat plants grown in the same soil and bacterial taxa were identified by sequencing prokaryote-specific 16S rRNA genes. Principal component analysis (PCA) of the sequencing data clearly separated wild and domesticated wheat varieties. Alpha diversity indices, which describe the diversity in microbial species and their abundance, were significantly higher for the domesticated cultivars, suggesting that domestication has increased endophyte diversity. While 110 bacterial genera were detected in both groups, albeit with differences in abundance, only one genus, Serratia, was unique to wild varieties and none were exclusive to domesticated cultivars. Serratia is known to enhance plant growth, particularly under salt stress and nutrient deprivation (Kulkova et al., 2024), and may be an important factor for wild wheat's stress resilience.
Based on significant pairwise correlations, the authors constructed bacterial interaction networks for both wheat groups (Figure 1a). Network connectivity (i.e., the number of co-occurrences) was higher for wild than domesticated wheat; domestication thus seems to have destabilised wheat's bacterial co-occurrence network. The analysis also identified several genera, including growth-promoting Chryseobacterium, Massilia and Lechevalieria, as keystone taxa that play central roles in these bacterial networks.
In parallel with their microbiome analysis, the authors generated metabolic profiles of root exudates from the six wheat varieties. Again, wild and domesticated wheat samples clustered separately in PCA, with eight and six metabolites found exclusively in wild and domesticated wheat, respectively. These findings indicate that domestication substantially altered root metabolism. The researchers integrated these metabolomics data with their microbiome data and detected significant correlations between keystone taxa and multiple metabolites. Among these, l-tyrosine stood out for its higher abundance in wild wheat roots and its strong correlation with the presence of Chryseobacterium. To explore this further, the team grew wheat plants in controlled conditions and exposed them to Chryseobacterium, l-tyrosine or a combination of both. While neither treatment altered shoot or root growth of domesticated wheat varieties, the combined exposure to l-tyrosine and Chryseobacterium reduced root elongation, but increased root fresh weight, of wild wheat (Figure 1b). Several Chryseobacterium species are known to promote plant growth by solubilising nutrients and producing plant hormones (Jung et al., 2023). The observations by Deng et al. support the hypothesis that wild wheat recruits or stimulates Chryseobacterium by the release of l-tyrosine, and that this beneficial relationship was lost during domestication.
Reshaping the microbiome represents a promising strategy for improving crop yield and resilience. Understanding how crops interact with their microbiomes, and how these interactions have changed through domestication, represents an important step towards this goal. The findings by Deng et al. highlight the potential of wild wheats and their microbiomes as valuable resources for improving modern wheat varieties. Bacteria such as Serratia and Chryseobacterium represent exciting candidates in this context, but changes to wheat's genetic make-up may be required to fully unlock the microbes' potential. Yue hopes that their studies will eventually lead to the development of microbial agents that can be applied in large-scale agricultural settings to enhance crop production.
期刊介绍:
Publishing the best original research papers in all key areas of modern plant biology from the world"s leading laboratories, The Plant Journal provides a dynamic forum for this ever growing international research community.
Plant science research is now at the forefront of research in the biological sciences, with breakthroughs in our understanding of fundamental processes in plants matching those in other organisms. The impact of molecular genetics and the availability of model and crop species can be seen in all aspects of plant biology. For publication in The Plant Journal the research must provide a highly significant new contribution to our understanding of plants and be of general interest to the plant science community.