玉米与叶际微生物组的互作遗传机制
收稿日期: 2022-10-31
录用日期: 2023-05-16
网络出版日期: 2023-05-17
基金资助
国家自然科学基金(31971398)
Genetic mechanism of interaction between maize and phyllospheric microbiome
Received date: 2022-10-31
Accepted date: 2023-05-16
Online published: 2023-05-17
Supported by
National Natural Science Foundation of China(31971398)
为了解玉米(Zea mays)和其定植微生物组之间的相互作用, 探究玉米与叶际微生物组之间的互作遗传机制, 该研究采用数学模型量化微生物之间相互作用的4种方式: 互利共生、拮抗、侵略、利他, 分析230份玉米叶际微生物组数据, 利用网络作图研究玉米与叶际微生物组之间的互作遗传机制。结果表明: 在微生物互作网络中确定了67个中心节点微生物, 通过网络作图筛选到玉米405个显著单核苷酸多态性(SNPs)位点, 最终定位到23个枢纽基因, 发现其在促进植物生长、抵御病原菌侵染、耐受非生物胁迫方面起到重要作用。研究结果有助于在作物遗传育种以及构建新型菌剂促进植物生长方面提供思路。
关键词： 玉米; 叶际微生物组; 网络作图; 中心节点微生物; 显著单核苷酸多态性(SNPs)位点
程可心 , 杜尧 , 李凯航 , 王浩臣 , 杨艳 , 金一 , 何晓青 . 玉米与叶际微生物组的互作遗传机制[J]. 植物生态学报, 2024 , 48(2) : 215 -228 . DOI: 10.17521/cjpe.2022.0433
Aims To understand the interaction between maize and its colonized microbiome, the genetic mechanism of interaction between maize and phyllospheric microbiome was explored.
Methods Four modes of interactions between microorganisms, including mutualistic symbiosis, antagonism, aggression, and altruism, were identified by using mathematical models. Based on 230 phyllospheric microbiome datasets of maize, network mapping was applied to characterize the interaction between maize and phyllospheric microbiome.
Important findings Sixty-seven hub microbes were identified in the microbial interaction network, 405 significant Single Nucleotide Polymorphisms in maize were screened through network mapping, and finally 23 hub genes were located, and it was found that they played an important role in promoting plant growth, resisting pathogenic bacteria infection and tolerating abiotic stresses.
| [1] | Asaf S, Numan M, Khan AL, Al-Harrasi A (2020). Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth. Critical Reviews in Biotechnology, 40, 138-152. |
| [2] | Barkan A, Small I (2014). Pentatricopeptide repeat proteins in plants. Annual Review of Plant Biology, 65, 415-442. |
| [3] | Batstone Rebecca T, O’brien Anna M, Harrison Tia L, Frederickson Megan E (2020). Experimental evolution makes microbes more cooperative with their local host genotype. Science, 370, 476-478. |
| [4] | Beilsmith K, Thoen MPM, Brachi B, Gloss AD, Khan MH, Bergelson J (2019). Genome-wide association studies on the phyllosphere microbiome: embracing complexity in host-microbe interactions. The Plant Journal, 97, 164-181. |
| [5] | Bergelson J, Mittelstrass J, Horton MW (2019). Characterizing both bacteria and fungi improves understanding of the Arabidopsis root microbiome. Scientific Reports, 9, 24. DOI: 10.1038/s41598-018-37208-z. |
| [6] | Brachi B, Filiault D, Darme P, Mentec M, Kerdaffrec E, Rabanal F, Anastasio A, Box M, Duncan S, Morton T, Novikova P, Perisin M, Tsuchimatsu T, Woolley R, Yu M, et al. (2017). Plant genes influence microbial hubs that shape beneficial leaf communities. bioRxiv. DOI: 10.1101/181198. |
| [7] | Brachi B, Filiault D, Whitehurst H, Darme P, Le Gars P, Le Mentec M, Morton TC, Kerdaffrec E, Rabanal F, Anastasio A, Box MS, Duncan S, Huang F, Leff R, Novikova P, et al. (2022). Plant genetic effects on microbial hubs impact host fitness in repeated field trials. Proceedings of the National Academy of Sciences of the United States of America, 119, e2201285119. DOI: 10.1073/pnas.2201285119. |
| [8] | Carrión VJ, Perez-Jaramillo J, Cordovez V, Tracanna V, de Hollander M, Ruiz-Buck D, Mendes LW, Gomez-Exposito R, Elsayed SS, Mohanraju P, Arifah A, van der Oost J, Paulson JN, Mendes R, et al. (2019). Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science, 366, 606-612. |
| [9] | Chen T, Nomura K, Wang XL, Sohrabi R, Xu J, Yao L, Paasch BC, Ma L, Kremer J, Cheng Y, Zhang L, Wang N, Wang E, Xin X, He S (2020). A plant genetic network for preventing dysbiosis in the phyllosphere. Nature, 580, 653-657. |
| [10] | de Vries FT, Griffiths RI, Knight CG, Nicolitch O, Williams A (2020). Harnessing rhizosphere microbiomes for drought- resilient crop production. Science, 368, 270-274. |
| [11] | Delaux P, Schornack S (2021). Plant evolution driven by interactions with symbiotic and pathogenic microbes. Science, 371, eaba6605. DOI: 10.1126/science.aba6605. |
| [12] | Deng S, Caddell DF, Xu G, Dahlen L, Washington L, Yang J, Coleman-Derr D (2021). Genome wide association study reveals plant loci controlling heritability of the rhizosphere microbiome. The ISME Journal, 15, 3181-3194. |
| [13] | Distéfano AM, Scuffi D, García-Mata C, Lamattina L, Laxalt AM (2012). Phospholipase δD is involved in nitric oxide-induced stomatal closure. Planta, 236, 1899-1907. |
| [14] | Escudero-Martinez C, Coulter M, Alegria Terrazas R, Foito A, Kapadia R, Pietrangelo L, Maver M, Sharma R, Aprile A, Morris J, Hedley PE, Maurer A, Pillen K, Naclerio G, Mimmo T, et al. (2022). Identifying plant genes shaping microbiota composition in the barley rhizosphere. Nature Communications, 13, 3443. DOI: 10.1038/s41467-022-31022-y. |
| [15] | Falbel TG, Koch LM, Nadeau JA, Segui-Simarro JM, Sack FD, Bednarek SY (2003). SCD1 is required for cell cytokinesis and polarized cell expansion in Arabidopsis thaliana. Development, 130, 4011-4024. |
| [16] | Figueiredo J, Sousa Silva M, Figueiredo A (2018). Subtilisin- like proteases in plant defence: the past, the present and beyond. Molecular Plant Pathology, 19, 1017-1028. |
| [17] | Finkel OM, Castrillo G, Herrera Paredes S, Salas González I, Dangl JL (2017). Understanding and exploiting plant beneficial microbes. Current Opinion in Plant Biology, 38, 155-163. |
| [18] | Gong TY, Xin XF (2021). Phyllosphere microbiota: community dynamics and its interaction with plant hosts. Journal of Integrative Plant Biology, 63, 297-304. |
| [19] | Hawkes CV, Kj?ller R, Raaijmakers JM, Riber L, Christensen S, Rasmussen S, Christensen JH, Dahl AB, Westergaard JC, Nielsen M, Brown-Guedira G, Hestbjerg Hansen L (2021). Extension of plant phenotypes by the foliar microbiome. Annual Review of Plant Biology, 72, 823-846. |
| [20] | He XQ, Zhang Q, Li BB, Jin Y, Jiang LB, Wu RL (2021). Network mapping of root-microbe interactions in Arabidopsis thaliana. NPJ Biofilms and Microbiomes, 7, 72. DOI: 10.1038/s41522-021-00241-4. |
| [21] | Horton MW, Bodenhausen N, Beilsmith K, Meng DZ, Muegge BD, Subramanian S, Vetter MM, Vilhjálmsson BJ, Nordborg M, Gordon JI, Bergelson J (2014). Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nature Communications, 5, 5320. DOI: 10.1038/ncomms6320. |
| [22] | Jiang L, Liu X, He X, Jin Y, Cao Y, Zhan X, Griffin CH, Gragnoli C, Wu R (2021). A behavioral model for mapping the genetic architecture of gut-microbiota networks. Gut Microbes, 13, 1820847. DOI: 10.1080/19490976.2020.1820847. |
| [23] | Li KH, Cheng KX, Wang HC, Zhang Q, Yang Y, Jin Y, He XQ, Wu RL (2022a). Disentangling leaf-microbiome interactions in Arabidopsis thaliana by network mapping. Frontiers in Plant Science, 13, 996121. DOI: 10.3389/fpls.2022.996121. |
| [24] | Li KH, Wang HC, Cheng KX, Yang Y, Jin Y, He XQ (2023). Genetic mechanisms of plant-microbiome interaction by genome-wide association analysis study. Biotechnology Bulletin, 39(2), 24-34. |
| [李凯航, 王浩臣, 程可心, 杨艳, 金一, 何晓青 (2023). 全基因组关联分析研究植物与微生物组的互作遗传机制. 生物技术通报, 39(2), 24-34.] | |
| [25] | Li PD, Zhu ZR, Zhang YZ, Xu JP, Wang HK, Wang ZY, Li HY (2022b). The phyllosphere microbiome shifts toward combating melanose pathogen. Microbiome, 10, 56. DOI: 10.1186/s40168-022-01234-x. |
| [26] | Li Z, Bai X, Jiao S, Li Y, Li P, Yang Y, Zhang H, Wei G (2021). A simplified synthetic community rescues Astragalus mongholicus from root rot disease by activating plant- induced systemic resistance. Microbiome, 9, 217. DOI: 10.1186/s40168-021-01169-9. |
| [27] | Madhaiyan M, Alex THH, Te Ngoh S, Prithiviraj B, Ji L (2015). Leaf-residing Methylobacterium species fix nitrogen and promote biomass and seed production in Jatropha curcas. Biotechnology for Biofuels, 8, 1-14. |
| [28] | Meier MA, Xu G, Lopez-Guerrero MG, Li G, Smith C, Sigmon B, Herr JR, Alfano JR, Ge Y, Schnable JC, Yang J (2022). Association analyses of host genetics, root- colonizing microbes, and plant phenotypes under different nitrogen conditions in maize. eLife, 11, 75790. DOI: 10.7554/eLife.75790. |
| [29] | Müller DB, Vogel C, Bai Y, Vorholt JA (2016). The plant microbiota: systems-level insights and perspectives. Annual Review of Genetics, 50, 211-234. |
| [30] | Oyserman BO, Flores SS, Griffioen T, Pan X, van der Wijk E, Pronk L, Lokhorst W, Nurfikari A, Paulson JN, Movassagh M, Stopnisek N, Kupczok A, Cordovez V, Carrión VJ, Ligterink W, et al. (2022). Disentangling the genetic basis of rhizosphere microbiome assembly in tomato. Nature Communications, 13, 3228. DOI: 10.1038/s41467-022-30849-9. |
| [31] | Pang Z, Chen J, Wang T, Gao C, Li Z, Guo L, Xu J, Cheng Y (2021). Linking plant secondary metabolites and plant microbiomes: a review. Frontiers in Plant Science, 12, 621276. DOI: 10.3389/fpls.2021.621276. |
| [32] | Roman-Reyna V, Pinili D, Borja FN, Quibod IL, Groen SC, Alexandrov N, Mauleon R, Oliva R (2020). Characterization of the leaf microbiome from whole-genome sequencing data of the 3000 rice genomes project. Rice, 13, 72. DOI: 10.1186/s12284-020-00432-1. |
| [33] | Schlaeppi K, Bulgarelli D (2015). The plant microbiome at work. Molecular Plant-Microbe Interactions, 28, 212-217. |
| [34] | Schmitz L, Yan Z, Schneijderberg M, de Roij M, Pijnenburg R, Zheng Q, Franken C, Dechesne A, Trindade LM, van Velzen R, Bisseling T, Geurts R, Cheng X (2022). Synthetic bacterial community derived from a desert rhizosphere confers salt stress resilience to tomato in the presence of a soil microbiome. The ISME Journal, 16, 1907-1920. |
| [35] | Stringlis IA, Yu K, Feussner K, de Jonge R, van Bentum S, van Verk MC, Berendsen RL, Bakker PAHM, Feussner I, Pieterse CMJ (2018). MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proceedings of the National Academy of Sciences of the United States of America, 115, E5213-E5222. |
| [36] | Tan XF, Xie HT, Yu JW, Wang YF, Xu JM, Xu P, Ma B (2022). Host genetic determinants drive compartment-specific assembly of tea plant microbiomes. Plant Biotechnology Journal, 20, 2174-2186. |
| [37] | Tong H, Zheng C, Li B, Swanner ED, Liu C, Chen M, Xia Y, Liu Y, Ning Z, Li F, Feng X (2021). Microaerophilic oxidation of Fe(II) coupled with simultaneous carbon fixation and As(III) oxidation and sequestration in karstic paddy soil. Environmental Science & Technology, 55, 3634-3644. |
| [38] | Trivedi P, Leach JE, Tringe SG, Sa TM, Singh BK (2020). Plant-microbiome interactions: from community assembly to plant health. Nature Reviews Microbiology, 18, 607-621. |
| [39] | Vogel CM, Potthoff DB, Sch?fer M, Barandun N, Vorholt JA (2021). Protective role of the Arabidopsis leaf microbiota against a bacterial pathogen. Nature Microbiology, 6, 1537-1548. |
| [40] | Wagner MR, Busby PE, Balint-Kurti P (2020). Analysis of leaf microbiome composition of near-isogenic maize lines differing in broad-spectrum disease resistance. New Phytologist, 225, 2152-2165. |
| [41] | Wallace JG, Kremling KA, Kovar LL, Buckler ES (2018). Quantitative genetics of the maize leaf microbiome. Phytobiomes Journal, 2, 208-224. |
| [42] | Wang CH, Li YJ, Li MJ, Zhang KF, Ma WJ, Zheng L, Xu HY, Cui BF, Liu R, Yang YQ, Zhong YJ, Liao H (2021). Functional assembly of root-associated microbial consortia improves nutrient efficiency and yield in soybean. Journal of Integrative Plant Biology, 63, 1021-1035. |
| [43] | Wang YY, Wang XL, Sun SA, Jin CZ, Su JM, Wei JP, Luo X, Wen JW, Wei T, Sahu SK, Zou HF, Chen HY, Mu ZX, Zhang GY, Liu X, et al. (2022). GWAS, MWAS and mGWAS provide insights into precision agriculture based on genotype- dependent microbial effects in foxtail millet. Nature Communications, 13, 5913. DOI: 10.1038/s41467-022-33238-4. |
| [44] | Wang ZH, Song Y (2022). Toward understanding the genetic bases underlying plant-mediated “cry for help” to the microbiota. iMeta, 1, e8. DOI: 10.1002/imt2.8. |
| [45] | Xie YH, Jia P, Zheng XT, Li JT, Shu WS, Wang YT (2022). Impacts and action pathways of domestication on diversity and community structure of crop microbiome: a review. Chinese Journal of Plant Ecology, 46, 249-266. |
| [谢育杭, 贾璞, 郑修坛, 李金天, 束文圣, 王宇涛 (2022). 驯化对作物微生物组多样性和群落结构的影响及作用途径. 植物生态学报, 46, 249-266.] | |
| [46] | Xiong C, Zhu YG, Wang JT, Singh B, Han LL, Shen JP, Li PP, Wang GB, Wu CF, Ge AH, Zhang LM, He JZ (2021). Host selection shapes crop microbiome assembly and network complexity. New Phytologist, 229, 1091-1104. |
| [47] | Yang K, Wang HL, Ye KH, Wang P, Meng GY, Luo C, Guo LW (2021). Advances in research on phyllosphere microorganisms and their interaction with plants. Journal of Yunnan Agricultural University (Natural Science), 36(1), 155-164. |
| [杨宽, 王慧玲, 叶坤浩, 王佩, 孟广云, 罗成, 郭力维 (2021). 叶际微生物及与植物互作的研究进展. 云南农业大学学报(自然科学), 36(1), 155-164.] | |
| [48] | Yin C, Casa Vargas JM, Schlatter DC, Hagerty CH, Hulbert SH, Paulitz TC (2021a). Rhizosphere community selection reveals bacteria associated with reduced root disease. Microbiome, 9, 86. DOI: 10.1186/s40168-020-00997-5. |
| [49] | Yin LL, Zhang HH, Tang ZS, Xu JY, Yin D, Zhang ZW, Yuan XH, Zhu MJ, Zhao SH, Li XY, Liu X (2021b). rMVP: a memory-efficient, visualization-enhanced, and parallel- accelerated tool for genome-wide association study. Genomics, Proteomics & Bioinformatics, 19, 619-628. |
| [50] | Zhang J, Liu Y, Guo X, Qin Y, Garrido-Oter R, Schulze-Lefert P, Bai Y (2021). High-throughput cultivation and identification of bacteria from the plant root microbiota. Nature Protocols, 16, 988-1012. |
| [51] | Zhang JY, Liu YX, Zhang N, Hu B, Jin T, Xu HR, Qin YA, Yan PX, Zhang XN, Guo XX, Hui J, Cao SY, Wang X, Wang C, Wang H, et al. (2019). NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nature Biotechnology, 37, 676-684. |
| [52] | Zhang LY, Zhang ML, Huang SY, Li LJ, Gao QA, Wang Y, Zhang SQ, Huang SM, Yuan LA, Wen YC, Liu KL, Yu XC, Li DC, Zhang L, Xu XP, et al. (2022). A highly conserved core bacterial microbiota with nitrogen-fixation capacity inhabits the xylem sap in maize plants. Nature Communications, 13, 3361. DOI: 10.1038/s41467-022-31113-w. |
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