Plant-Microbiome Interactions：An Eco-Evolutionary Perspective

doi:10.13560/j.cnki.biotech.bull.1985.2020-0978

Abstract

Abstract: Microorganisms thriving at the plant surfaces and internal tissues play critical roles in plant growth,development,adaptation,and diversification. Numerous studies have revealed the great functional capacity of plant-associated microbiome,however,it is not clear how plant-associated microbiome assembles in plant evolutionary process. In this paper,the ecological adaptation and the evolutionary mechanism of plant-microbiome interactions are summarized based on the evolutionary trajectory of plant phylogeny,plant-microbiome in crop domestication,and the microbe-microbe interaction and evolution under host constraints. Understanding the evolutionary drivers of plant-microbiome interactions may contribute to restoring the beneficial connections between plants and microbes,thus achieving the goals of high yield and high efficiency by increasing crop nutrient absorption,yield and quality. Strengthening the strategy of combining molecular biology and crop genomics will be the key to regulate plant microbiome to promote agricultural sustainability. Meanwhile,the outlook of eco-evolutionary of plant-microbiome interactions is highlighted.

Key words: phylogenetic, domestication, holobiont, eco-evolutionary, sustainable agriculture

CHENG Sai-sai, GONG Xin, XUE Wen-feng, WAN Bing-bing, LIU Man-qiang, HU Feng. Plant-Microbiome Interactions：An Eco-Evolutionary Perspective[J]. Biotechnology Bulletin, 2020, 36(9): 3-13.

References

[1] Field KJ, Pressel S, Duckett JG, et al.Symbiotic options for the conquest of land[J]. Trends in Ecology & Evolution, 2015, 30(8):477-486.
[2] Zilber-Rosenberg I, Rosenberg E.Role of microorganisms in the evolution of animals and plants:the hologenome theory of evolution[J]. FEMS Microbiol Rev, 2008, 32(5):723-735.
[3] Lugtenberg B, Kamilova F.Plant-growth-promoting rhizobacteria[J]. Annual Review of Microbiology, 2009, 63(1):541-556.
[4] 孙真, 郑亮, 邱浩斌. 植物根际促生细菌定殖研究进展[J]. 生物技术通报, 2017, 33(2):8-15.
Sun Z, Zhen L, Qiu HB.Research advances on colonization of plant growth-promoting rhizobacteria[J]. Biotechnology Bulletin, 2017, 33(2):8-15.
[5] Verbon EH, Liberman LM.Beneficial microbes affect endogenous mechanisms controlling root development[J]. Trends Plant Sci, 2016, 21(3):218-229.
[6] Berendsen RL, Pieterse CM, Bakker PA.The rhizosphere microbiome and plant health[J]. Trends Plant Sci, 2012, 17(8):478-486.
[7] Liu H, Brettell LE, Qiu Z, et al.Microbiome-mediated stress resistance in plants[J]. Trends Plant Sci, 2020, 25(8):733-743.
[8] 姜焕焕, 王通, 陈娜, 等. 根际促生菌提高植物抗盐碱性的研究进展[J]. 生物技术通报, 2019, 35(10):189-197.
Jiang HH, Wang T, Chen N, et al.Research progress in PGPR improving plant’s resistance to salt and alkali[J]. Biotechnology Bulletin, 2019, 35(10):189-197.
[9] Mendes R, Garbeva P, Raaijmakers JM.The rhizosphere microbiome:significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms[J]. FEMS Microbiology Reviews, 2013, 37(5):634-663.
[10] 王端, 姚香梅, 叶健. 根际微生物-植物-病毒-介体昆虫多元互作研究进展[J]. 生物技术通报, 2018, 34(2):54-65.
Wang D, Yao XM, Ye J.Research progress on multipartite interactions among rhizosphere microbe-plants-virus-vector insect[J]. Biotechnology Bulletin, 2018, 34(2):54-65.
[11] Schlaeppi K, Bulgarelli D.The plant microbiome at work[J]. Mol Plant Microbe Interact, 2015, 28(3):212-217.
[12] Hacquard S, Garrido-Oter R, Gonzalez A, et al.Microbiota and Host Nutrition across Plant and Animal Kingdoms[J]. Cell Host Microbe, 2015, 17(5):603-616.
[13] Fitzpatrick CR, Copeland J, Wang PW, et al.Assembly and ecological function of the root microbiome across angiosperm plant species[J]. Proc Natl Acad Sci USA, 2018, 115(6):1157-1165.
[14] Gordon J, Youle M, Knowlton N, et al.Superorganisms and Holobionts[J]. Microbe, 2013, 8(4):152-153.
[15] Sasse J, Martinoia E, Northen T.Feed your friends:do plant exudates shape the root microbiome?[J]. Trends Plant Sci, 2018, 23(1):25-41.
[16] Foster KR, Schluter J, Coyte KZ, et al.The evolution of the host microbiome as an ecosystem on a leash[J]. Nature, 2017, 548(7665):43-51.
[17] Panke-Buisse K, Poole AC, Goodrich JK, et al.Selection on soil microbiomes reveals reproducible impacts on plant function[J]. The ISME Journal, 2015, 9(4):980-989.
[18] 焦健, 田长富. 根瘤菌共生固氮能力的进化模式[J]. 微生物学通报, 2019, 46(2):388-397.
Jiao J, Tian CF.Evolution of rhizobial nodulation and nitrogen fixation[J]. Microbiology, 2019, 46(2):388-397.
[19] Gilbert GS, Parker IM.The evolutionary ecology of plant disease:a phylogenetic perspective[J]. Annu Rev Phytopathol, 2016, 54:549-578.
[20] Bouffaud ML, Poirier MA, Muller D, et al.Root microbiome relates to plant host evolution in maize and other Poaceae[J]. Environ Microbiol, 2014, 16(9):2804-2814.
[21] Yang T, Tedersoo L, Soltis PS, et al.Phylogenetic imprint of woody plants on the soil mycobiome in natural mountain forests of eastern China[J]. The ISME Journal, 2019, 13(3):686-697.
[22] Gilbert GS, Webb CO.Phylogenetic signal in plant pathogen-host range[J]. Proc Natl Acad Sci USA, 2007, 104(12):4979-4983.
[23] Yeoh YK, Dennis PG, Paungfoo-Lonhienne C, et al.Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence[J]. Nature Communications, 2017, 8(1):1-9.
[24] Naylor D, DeGraaf S, Purdom E, et al. Drought and host selection influence bacterial community dynamics in the grass root microbiome[J]. The ISME Journal, 2017, 11(12):2691-2704.
[25] Escudero-Martinez C, Bulgarelli D.Tracing the evolutionary routes of plant-microbiota interactions[J]. Curr Opin Microbiol, 2019, 4934-4940.
[26] Purugganan MD, Fuller DQ.The nature of selection during plant domestication[J]. Nature, 2009, 457(7231):843-848.
[27] Milla R, Osborne CP, Turcotte MM, et al.Plant domestication through an ecological lens[J]. Trends in Ecology & Evolution, 2015, 30(8):463-469.
[28] Wissuwa M, Mazzola M, Picard C.Novel approaches in plant breeding for rhizosphere-related traits[J]. Plant Soil, 2009, 321(1-2):409-430.
[29] Vandenkoornhuyse P, Quaiser A, Duhamel M, et al.The importance of the microbiome of the plant holobiont[J]. New Phytol, 2015, 206(4):1196-1206.
[30] Kiers ET, Denison RF.Inclusive fitness in agriculture[J]. Phil Trans R Soc B, 2014, 369(1642):20130367.
[31] 常春玲, 马丽娜, 田春杰. 作物驯化对根际微生物组的选择效应[J]. 土壤与作物, 2018, 7(2):236-241.
Chang CL, Ma LN, Tian CJ.A selecting effect of crop domestication on rhizomicrobiome[J]. Soil and Crop, 2018, 7(2):236-241.
[32] Mutch LA, Young JP.Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes[J]. Molecular Ecology, 2004, 13(8):2435-2444.
[33] Kiers ET, Hutton MG, Denison RF.Human selection and the relaxation of legume defences against ineffective rhizobia[J]. Phil Trans R Soc B, 2007, 274(1629):3119-3126.
[34] Sangabriel-Conde W, Negrete-Yankelevich S, Maldonado-Mendoza IE, et al.Native maize landraces from Los Tuxtlas, Mexico show varying mycorrhizal dependency for P uptake[J]. Biology and Fertility of Soils, 2013, 50(2):405-414.
[35] Hetrick BAD, Wilson GWT, Gill BS, et al.Chromosome location of mycorrhizal responsive genes in wheat[J]. Canadian Journal of Botany, 1995, 73(6):891-897.
[36] Zachow C, Muller H, Tilcher R, et al.Differences between the rhizosphere microbiome of Beta vulgaris ssp. maritima-ancestor of all beet crops-and modern sugar beets[J]. Front Microbiol, 2014, 5:415.
[37] Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, et al.Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species[J]. New Phytol, 2016, 209
(2):798-811.
[38] Bulgarelli D, Garrido-Oter R, Munch PC, et al.Structure and function of the bacterial root microbiota in wild and domesticated barley[J]. Cell Host Microbe, 2015, 17(3):392-403.
[39] Perez-Jaramillo JE, Carrion VJ, Bosse M, et al.Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits[J]. The ISME Journal, 2017, 11(10):2244-2257.
[40] Zancarini A, Mougel C, Voisin AS, et al.Soil nitrogen availability and plant genotype modify the nutrition strategies of M. truncatula and the associated rhizosphere microbial communities[J]. Plos One, 2012, 7(10):e47096.
[41] Verbruggen E, Toby Kiers E.Evolutionary ecology of mycorrhizal functional diversity in agricultural systems[J]. Evol Appl, 2010, 3(5-6):547-560.
[42] Duhamel M, Vandenkoornhuyse P.Sustainable agriculture:possible trajectories from mutualistic symbiosis and plant neodomestication[J]. Trends Plant Sci, 2013, 18(11):597-600.
[43] Weese DJ, Heath KD, Dentinger BT, et al.Long-term nitrogen addition causes the evolution of less-cooperative mutualists[J]. Evolution, 2015, 69(3):631-642.
[44] Ramirez KS, Craine JM, Fierer N.Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes[J]. Global Change Biology, 2012, 18(6):1918-1927.
[45] Perez-Jaramillo JE, Mendes R, Raaijmakers JM.Impact of plant domestication on rhizosphere microbiome assembly and functions[J]. Plant Mol Biol, 2016, 90(6):635-644.
[46] Cordovez V, Dini-Andreote F, Carrion VJ, et al.Ecology and evolution of plant microbiomes[J]. Annual Review of Microbiology, 2019, 7369-88.
[47] Werner GDA, Cornelissen JHC, Cornwell WK, et al.Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown[J]. Proc Natl Acad Sci USA, 2018, 115(20):5229-5234.
[48] Perez-Jaramillo JE, Carrion VJ, de Hollander M, et al. The wild side of plant microbiomes[J]. Microbiome, 2018, 6(1):143-148.
[49] Chen L, Zheng Y, Gao C, et al.Phylogenetic relatedness explains highly interconnected and nested symbiotic networks of woody plants and arbuscular mycorrhizal fungi in a Chinese subtropical forest[J]. Mol Ecol, 2017, 26(9):2563-2575.
[50] Montesinos-Navarro A, Segarra-Moragues JG, Valiente-Banuet A, et al.Plant facilitation occurs between species differing in their associated arbuscular mycorrhizal fungi[J]. New Phytol, 2012, 196(3):835-844.
[51] Hassani MA, Duran P, Hacquard S.Microbial interactions within the plant holobiont[J]. Microbiome, 2018, 6(1):58-74.
[52] Chisholm ST, Coaker G, Day B, et al.Host-microbe interactions:shaping the evolution of the plant immune response[J]. Cell, 2006, 124(4):803-814.
[53] Benizri E, Nguyen C, Piutti S, et al.Additions of maize root mucilage to soil changed the structure of the bacterial community[J]. Soil Biology & Biochemistry, 2007, 39(5):1230-1233.
[54] Gundel PE, Rudgers JA, Ghersa CM.Incorporating the process of vertical transmission into understanding of host-symbiont dynamics[J]. Oikos, 2011, 120(8):1121-1128.
[55] Mee MT, Collins JJ, Church GM, et al.Syntrophic exchange in synthetic microbial communities[J]. Proc Natl Acad Sci USA, 2014, 111(20):2149-2156.
[56] Morris BE, Henneberger R, Huber H, et al.Microbial syntrophy:interaction for the common good[J]. FEMS Microbiol Rev, 2013, 37(3):384-406.
[57] Harcombe W.Novel cooperation experimentally evolved between species[J]. Evolution, 2010, 64(7):2166-2172.
[58] Peterson SB, Dunn AK, Klimowicz AK, et al.Peptidoglycan from Bacillus cereus mediates commensalism with rhizosphere bacteria from the Cytophaga-Flavobacterium group[J]. Applied and Environmental Microbiology, 2006, 72(8):5421-5427.
[59] Mas A, Jamshidi S, Lagadeuc Y, et al.Beyond the black queen Hypothesis[J]. The ISME Journal, 2016, 10(9):2085-2091.
[60] Gu SH, Wei Z, Shao ZY, et al.Competition for iron drives phytopathogen control by natural rhizosphere microbiomes[J]. Nature Microbiology, 2020, 5(8):1002-1010.
[61] Wandersman C, Delepelaire P.Bacterial iron sources:from siderophores to hemophores[J]. Annual Review of Microbiology, 2004, 58:611-647.
[62] Little AE, Robinson CJ, Peterson SB, et al.Rules of engagement:interspecies interactions that regulate microbial communities[J]. Annual Review of Microbiology, 2008, 62:375-401.
[63] Whipps JM.Microbial interactions and biocontrol in the rhizosphere[J]. J Exp Bot, 2001, 52:487-511.
[64] Friesen ML, Porter SS, Stark SC, et al.Microbially mediated plant functional traits[J]. Annual Review of Ecology, Evolution, and Systematics, 2011, 42(1):23-46.
[65] Mercado-Blanco J, Bakker PA.Interactions between plants and beneficial Pseudomonas spp. :exploiting bacterial traits for crop protection[J]. Antonie Van Leeuwenhoek, 2007, 92(4):367-389.
[66] Wei Z, Yang T, Friman VP, et al.Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health[J]. Nature Communications, 2015, 6(1):1-9.
[67] Leveau JH, Preston GM.Bacterial mycophagy:definition and diagnosis of a unique bacterial-fungal interaction[J]. New Phytol, 2008, 177(4):859-876.
[68] Barnett HL.The nature of mycoparasitism by fungi[J]. Annual Reviews in Microbiology, 1963, 17(1):1-14.
[69] Taylor TN, Winfried Remy, Hass. H.Fungi from the Lower Devonian Rhynie chert:Chytridiomycetes[J]. American Journal of Botany, 1992, 79(11):1233-1241.
[70] Xiong W, Song Y, Yang K, et al.Rhizosphere protists are key determinants of plant health[J]. Microbiome, 2020, 8(1):27-35.
[71] Jousset A, Rochat L, Scheu S, et al.Predator-prey chemical warfare determines the expression of biocontrol genes by rhizosphere-associated Pseudomonas fluorescens[J]. Applied and Environmental Microbiology, 2010, 76(15):5263-5268.
[72] Flues S, Bass D, Bonkowski M.Grazing of leaf-associated Cercomonads(Protists:Rhizaria:Cercozoa)structures bacterial community composition and function[J]. Environmental Microbiology, 2017, 19(8):3297-3309.
[73] Steffan SA, Chikaraishi Y, Currie CR, et al.Microbes are trophic analogs of animals[J]. Proc Natl Acad Sci USA, 2015, 112(49):15119-15124.
[74] Niu B, Paulson JN, Zheng X, et al.Simplified and representative bacterial community of maize roots[J]. Proc Natl Acad Sci USA, 2017, 114(12):2450-2459.
[75] Robertson GP, Vitousek PM.Nitrogen in agriculture:balancing the cost of an essential resource[J]. Annual Review of Environment and Resources, 2009, 34(1):97-125.
[76] Kirtman B, Power SB, Adedoyin JA, et al.Near-term climate change:Projections and predictability// Climate change 2013:in The Physical Science Basis:Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, ed. by Change Intergovernmental Panel on Climate[C]. Cambridge:Cambridge University Press, 2013.
[77] Challinor AJ, Watson J, Lobell DB, et al.A meta-analysis of crop yield under climate change and adaptation[J]. Nature Climate Change, 2014, 4(4):287-291.
[78] Bommarco R, Kleijn D, Potts SG.Ecological intensification:harnessing ecosystem services for food security[J]. Trends in Ecology & Evolution, 2013, 28(4):230-238.
[79] Griffiths B, Faber J, Bloem J.Applying soil health indicators to encourage sustainable soil use:the transition from scientific study to practical application[J]. Sustainability, 2018, 10(9):3021-3034.
[80] Jackson LE, Bowles TM, Hodson AK, et al.Soil microbial-root and microbial-rhizosphere processes to increase nitrogen availability and retention in agroecosystems[J]. Current Opinion in Environmental Sustainability, 2012, 4(5):517-522.
[81] Schmidt JE, Bowles TM, Gaudin AC.Using ancient traits to convert soil health into crop yield:impact of selection on maize root and rhizosphere function[J]. Frontiers in Plant Science, 2016, 7:373.
[82] Lipper L, Thornton P, Campbell BM, et al.Climate-smart agriculture for food security[J]. Nature Climate Change, 2014, 4(12):1068-1072.
[83] 杨新萍, 于媛, 许操. 重新设计与快速驯化创造新型作物[J]. 遗传, 2019, 41(9):827-835.
Yang XP, Yu Y, Xu C.De novo domestication to create new crops[J]. Hereditas(Beijing), 2019, 41(9):827-835.
[84] York LM, Galindo-Castaneda T, Schussler JR, et al.Evolution of US maize(Zea mays L.)root architectural and anatomical phenes over the past 100 years corresponds to increased tolerance of nitrogen stress[J]. J Exp Bot, 2015, 66(8):2347-2358.
[85] Duvick DN.The contribution of breeding to yield advances in maize(Zea mays L.)[J], Advances in Agronomy, 2005, 86:83-145.
[86] Horton MW, Bodenhausen N, Beilsmith K, et al.Genome-wide association study of Arabidopsis thaliana leaf microbial community[J]. Nature Communications, 2014, 5(1):1-7.
[87] Wallace JG, Kremling KA, Kovar LL, et al.Quantitative genetics of the maize leaf microbiome[J]. Phytobiomes Journal, 2018, 2(4):208-224.
[88] Wagner MR, Roberts JH, Balint-Kurti P, et al.Heterosis of leaf and rhizosphere microbiomes in field-grown maize[J]. New Phytol, 2020.
[89] Huang AC, Jiang T, Liu YX, et al. A specialized metabolic network selectively modulates Arabidopsis root microbiota[J]. Science, 2019, 364(6440):eaau6389.
[90] Mendes LW, Raaijmakers JM, de Hollander M, et al. Influence of resistance breeding in common bean on rhizosphere microbiome composition and function[J]. The ISME Journal, 2018, 12(1):212-224.
[91] Cermak T, Curtin SJ, Gil-Humanes J, et al.A multipurpose toolkit to enable advanced genome engineering in plants[J]. Plant Cell, 2017, 29(6):1196-1217.
[92] 景润春, 卢洪. CRISPR/Cas9基因组定向编辑技术的发展与在作物遗传育种中的应用[J]. 中国农业科学, 2016, 49(7):1219-1229.
Jing RC, Lu H.The development of CRISPR/Cas9 system and its application in crop genome editing[J]. Scientia Agricultura Sinica, 2016, 49(7):1219-1229.
[93] Zsogon A, Cermak T, Naves ER, et al.De novo domestication of wild tomato using genome editing[J]. Nature Biotechnology, 2018, 36:1211-1216.
[94] Ghosh S, Watson A, Gonzalez-Navarro OE, et al.Speed breeding in growth chambers and glasshouses for crop breeding and model plant research[J]. Nature Protocols, 2018, 13(12):2944-2963.
[95] 白洋, 钱景美, 周俭民, 等. 农作物微生物组:跨越转化临界点的现代生物技术[J]. 中国科学院院刊, 2017, 32(3):260-265.
Bai Y, Qian JM, Zhou JM, et al.Crop microbiome:Breakthrough technology for agriculture[J]. Bulletin of Chinese Academy of Sciences, 2017, 32(3):260-265.