1932

Abstract

The microbiota populating the plant–soil continuum defines an untapped resource for sustainable crop production. The host plant is a driver for the taxonomic composition and function of these microbial communities. In this review, we illustrate how the host genetic determinants of the microbiota have been shaped by plant domestication and crop diversification. We discuss how the heritable component of microbiota recruitment may represent, at least partially, a selection for microbial functions underpinning the growth, development, and health of their host plants and how the magnitude of this heritability is influenced by the environment. We illustrate how host–microbiota interactions can be treated as an external quantitative trait and review recent studies associating crop genetics with microbiota-based quantitative traits. We also explore the results of reductionist approaches, including synthetic microbial communities, to establish causal relationships between microbiota and plant phenotypes. Lastly, we propose strategies to integrate microbiota manipulation into crop selection programs. Although a detailed understanding of when and how heritability for microbiota composition can be deployed for breeding purposes is still lacking, we argue that advances in crop genomics are likely to accelerate wider applications of plant–microbiota interactions in agriculture.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-021621-121447
2023-09-05
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/phyto/61/1/annurev-phyto-021621-121447.html?itemId=/content/journals/10.1146/annurev-phyto-021621-121447&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abbo S, van-Oss RP, Gopher A, Saranga Y, Ofner I, Peleg Z. 2014. Plant domestication versus crop evolution: a conceptual framework for cereals and grain legumes. Trends Plant Sci. 19:351–60
    [Google Scholar]
  2. 2.
    Agler MT, Ruhe J, Kroll S, Morhenn C, Kim S-T et al. 2016. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLOS Biol. 14:e1002352
    [Google Scholar]
  3. 3.
    Alegria Terrazas R, Balbirnie-Cumming K, Morris J, Hedley PE, Russell J et al. 2020. A footprint of plant eco-geographic adaptation on the composition of the barley rhizosphere bacterial microbiota. Sci. Rep. 10:12916
    [Google Scholar]
  4. 4.
    Alegria Terrazas R, Robertson-Albertyn S, Corral AM, Escudero-Martinez C, Kapadia R et al. 2022. Defining composition and function of the rhizosphere microbiota of barley genotypes exposed to growth-limiting nitrogen supplies. mSystems 7:6e00934–22
    [Google Scholar]
  5. 5.
    Balint-Kurti P, Simmons SJ, Blum JE, Ballaré CL, Stapleton AE. 2010. Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. Mol. Plant-Microbe Interact. 23:473–84
    [Google Scholar]
  6. 6.
    Bergelson J, Mittelstrass J, Horton MW. 2019. Characterizing both bacteria and fungi improves understanding of the Arabidopsis root microbiome. Sci. Rep. 9:24
    [Google Scholar]
  7. 7.
    Bodenhausen N, Bortfeld-Miller M, Ackermann M, Vorholt JA. 2014. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLOS Genet. 10:e1004283First example of the use of SynComs to dissect the plant genetic control of the microbiota.
    [Google Scholar]
  8. 8.
    Borojevic K, Borojevic K. 2005. The transfer and history of “reduced height genes”(Rht) in wheat from Japan to Europe. J. Hered. 96:455–59
    [Google Scholar]
  9. 9.
    Brachi B, Filiault D, Whitehurst H, Darme P, Le Gars P et al. 2022. Plant genetic effects on microbial hubs impact host fitness in repeated field trials. PNAS 119:e2201285119
    [Google Scholar]
  10. 10.
    Brader G, Compant S, Vescio K, Mitter B, Trognitz F et al. 2017. Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu. Rev. Phytopathol. 55:61–83
    [Google Scholar]
  11. 11.
    Brisson VL, Schmidt JE, Northen TR, Vogel JP, Gaudin ACM. 2019. Impacts of maize domestication and breeding on rhizosphere microbial community recruitment from a nutrient depleted agricultural soil. Sci. Rep. 9:15611
    [Google Scholar]
  12. 12.
    Bulgarelli D, Garrido-Oter R, Münch Philipp C, Weiman A, Dröge J et al. 2015. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403
    [Google Scholar]
  13. 13.
    Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P. 2013. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64:807–38
    [Google Scholar]
  14. 14.
    Cadot S, Guan H, Bigalke M, Walser J-C, Jander G et al. 2021. Specific and conserved patterns of microbiota-structuring by maize benzoxazinoids in the field. Microbiome 9:103
    [Google Scholar]
  15. 15.
    Canarini A, Kaiser C, Merchant A, Richter A, Wanek W. 2019. Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front. Plant Sci. 10:157
    [Google Scholar]
  16. 16.
    Carrión VJ, Perez-Jaramillo J, Cordovez V, Tracanna V, de Hollander M et al. 2019. Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366:606–12
    [Google Scholar]
  17. 17.
    Chai X, Wang X, Pi Y, Wu T, Zhang X et al. 2022. MdNRT2.4 interacts with rhizosphere bacteria to enhance nitrate uptake in apple rootstocks. J. Exp. Bot. 73:186490–504
    [Google Scholar]
  18. 18.
    Charpentier M, Oldroyd G. 2010. How close are we to nitrogen-fixing cereals?. Curr. Opin. Plant Biol. 13:556–64
    [Google Scholar]
  19. 19.
    Cordovez V, Dini-Andreote F, Carrion VJ, Raaijmakers JM. 2019. Ecology and evolution of plant microbiomes. Annu. Rev. Microbiol. 73:69–88
    [Google Scholar]
  20. 20.
    Cotton T, Pétriacq P, Cameron DD, Meselmani MA, Schwarzenbacher R et al. 2019. Metabolic regulation of the maize rhizobiome by benzoxazinoids. ISME J. 13:1647–58
    [Google Scholar]
  21. 21.
    Dayan FE, Rimando AM, Pan Z, Baerson SR, Gimsing AL, Duke SO. 2010. Sorgoleone. Phytochemistry 71:1032–39
    [Google Scholar]
  22. 22.
    Della Coletta R, Qiu Y, Ou S, Hufford MB, Hirsch CN 2021. How the pan-genome is changing crop genomics and improvement. Genome Biol. 22:3
    [Google Scholar]
  23. 23.
    Deng S, Caddell DF, Xu G, Dahlen L, Washington L et al. 2021. Genome wide association study reveals plant loci controlling heritability of the rhizosphere microbiome. ISME J. 15:3181–94Compelling example of genome-wide association study for rhizosphere microbiota data conducted in crops.
    [Google Scholar]
  24. 24.
    Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK et al. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. PNAS 112:E911–20
    [Google Scholar]
  25. 25.
    Elbeltagy A, Nishioka K, Suzuki H, Sato T, Sato Y-I et al. 2000. Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci. Plant Nutr. 46:617–29
    [Google Scholar]
  26. 26.
    Escudero-Martinez C, Bulgarelli D. 2019. Tracing the evolutionary routes of plant–microbiota interactions. Curr. Opin. Microbiol. 49:34–40
    [Google Scholar]
  27. 27.
    Escudero-Martinez C, Coulter M, Alegria Terrazas R, Foito A, Kapadia R et al. 2022. Identifying plant genes shaping microbiota composition in the barley rhizosphere. Nat. Commun. 13:3443Compelling example of how microbiota data can be treated as a quantitative trait in wild and domesticated barley genotypes.
    [Google Scholar]
  28. 28.
    Favela A, Bohn M, Kent A. 2022. N-cycling microbiome recruitment differences between modern and wild Zea mays. Phytobiomes J. 6:2151–60
    [Google Scholar]
  29. 29.
    Favela A, Bohn MO, Kent AD. 2021. Maize germplasm chronosequence shows crop breeding history impacts recruitment of the rhizosphere microbiome. ISME J. 15:2454–64
    [Google Scholar]
  30. 30.
    Fitzpatrick CR, Salas-González I, Conway JM, Finkel OM, Gilbert S et al. 2020. The plant microbiome: from ecology to reductionism and beyond. Annu. Rev. Microbiol. 74:81–100
    [Google Scholar]
  31. 31.
    Grün S, Frey M, Gierl A. 2005. Evolution of the indole alkaloid biosynthesis in the genus Hordeum: distribution of gramine and DIBOA and isolation of the benzoxazinoid biosynthesis genes from Hordeum lechleri. Phytochemistry 66:1264–72
    [Google Scholar]
  32. 32.
    Guo J, Ling N, Li Y, Li K, Ning H et al. 2021. Seed-borne, endospheric and rhizospheric core microbiota as predictors of plant functional traits across rice cultivars are dominated by deterministic processes. New Phytol. 230:2047–60
    [Google Scholar]
  33. 33.
    Hacquard S, Garrido-Oter R, González A, Spaepen S, Ackermann G et al. 2015. Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17:603–16
    [Google Scholar]
  34. 34.
    Hassani MA, Özkurt E, Seybold H, Dagan T, Stukenbrock EH. 2019. Interactions and coadaptation in plant metaorganisms. Annu. Rev. Phytopathol. 57:483–503
    [Google Scholar]
  35. 35.
    Herrera Paredes S, Gao T, Law TF, Finkel OM, Mucyn T et al. 2018. Design of synthetic bacterial communities for predictable plant phenotypes. PLOS Biol. 16:e2003962
    [Google Scholar]
  36. 36.
    Horton MW, Bodenhausen N, Beilsmith K, Meng D, Muegge BD et al. 2014. Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nat. Commun. 5:5320
    [Google Scholar]
  37. 37.
    Hu L, Robert CA, Cadot S, Zhang X, Ye M et al. 2018. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9:2738
    [Google Scholar]
  38. 38.
    Huang X, Kurata N, Wang Z-X, Wang A, Zhao Q et al. 2012. A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501
    [Google Scholar]
  39. 39.
    Jacoby RP, Koprivova A, Kopriva S. 2021. Pinpointing secondary metabolites that shape the composition and function of the plant microbiome. J. Exp. Bot. 72:57–69
    [Google Scholar]
  40. 40.
    Johnston-Monje D, Gutiérrez JP, Lopez-Lavalle LAB. 2021. Seed-transmitted bacteria and fungi dominate juvenile plant microbiomes. Front. Microbiol. 12:737616
    [Google Scholar]
  41. 41.
    Johnston-Monje D, Raizada MN. 2011. Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLOS ONE 6:e20396
    [Google Scholar]
  42. 42.
    Jupe F, Witek K, Verweij W, Śliwka J, Pritchard L et al. 2013. Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J. 76:530–44
    [Google Scholar]
  43. 43.
    Kavamura VN, Robinson RJ, Hughes D, Clark I, Rossmann M et al. 2020. Wheat dwarfing influences selection of the rhizosphere microbiome. Sci. Rep. 10:1452
    [Google Scholar]
  44. 44.
    Kim H, Jeon J, Lee KK, Lee Y-H. 2022. Longitudinal transmission of bacterial and fungal communities from seed to seed in rice. Commun. Biol. 5:772
    [Google Scholar]
  45. 45.
    Koprivova A, Schuck S, Jacoby RP, Klinkhammer I, Welter B et al. 2019. Root-specific camalexin biosynthesis controls the plant growth-promoting effects of multiple bacterial strains. PNAS 116:15735–44
    [Google Scholar]
  46. 46.
    Kudjordjie EN, Sapkota R, Steffensen SK, Fomsgaard IS, Nicolaisen M. 2019. Maize synthesized benzoxazinoids affect the host associated microbiome. Microbiome 7:59
    [Google Scholar]
  47. 47.
    Kwak M-J, Kong HG, Choi K, Kwon S-K, Song JY et al. 2018. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat. Biotechnol. 36:1100–9
    [Google Scholar]
  48. 48.
    Langridge P, Waugh R. 2019. Harnessing the potential of germplasm collections. Nat. Genet. 51:200–1
    [Google Scholar]
  49. 49.
    Leff JW, Lynch RC, Kane NC, Fierer N. 2017. Plant domestication and the assembly of bacterial and fungal communities associated with strains of the common sunflower, Helianthus annuus. New Phytol. 214:412–23
    [Google Scholar]
  50. 50.
    Li J, Wang J, Liu H, Macdonald CA, Singh BK. 2022. Application of microbial inoculants significantly enhances crop productivity: a meta-analysis of studies from 2010 to 2020. J. Sustain. Agric. Environ. 1:216–25
    [Google Scholar]
  51. 51.
    Lin X, Armstrong M, Baker K, Wouters D, Visser RG et al. 2020. RLP/K enrichment sequencing; a novel method to identify receptor-like protein (RLP) and receptor-like kinase (RLK) genes. New Phytol. 227:1264–76
    [Google Scholar]
  52. 52.
    Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63:541–56
    [Google Scholar]
  53. 53.
    Matsumoto H, Fan X, Wang Y, Kusstatscher P, Duan J et al. 2021. Bacterial seed endophyte shapes disease resistance in rice. Nat. Plants 7:60–72
    [Google Scholar]
  54. 54.
    Maver M, Escudero-Martinez C, Abbott J, Morris J, Hedley PE et al. 2021. Applications of the indole-alkaloid gramine modulate the assembly of individual members of the barley rhizosphere microbiota. PeerJ 9:e12498
    [Google Scholar]
  55. 55.
    Maver M, Miras-Moreno B, Lucini L, Trevisan M, Pii Y et al. 2020. New insights in the allelopathic traits of different barley genotypes: Middle Eastern and Tibetan wild-relative accessions versus cultivated modern barley. PLOS ONE 15:e0231976
    [Google Scholar]
  56. 56.
    Meier MA, Xu G, Lopez-Guerrero MG, Li G, Smith C et al. 2022. Association analyses of host genetics, root-colonizing microbes, and plant phenotypes under different nitrogen conditions in maize. eLife 11:e75790
    [Google Scholar]
  57. 57.
    Mitter B, Pfaffenbichler N, Flavell R, Compant S, Antonielli L et al. 2017. A new approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds. Front. Microbiol. 8:11
    [Google Scholar]
  58. 58.
    Neal J, Larson RI, Atkinson T. 1973. Changes in rhizosphere populations of selected physiological groups of bacteria related to substitution of specific pairs of chromosomes in spring wheat. Plant Soil 39:209–12
    [Google Scholar]
  59. 59.
    Nerva L, Sandrini M, Moffa L, Velasco R, Balestrini R, Chitarra W. 2022. Breeding toward improved ecological plant–microbiome interactions. Trends Plant Sci. 27:111134–43
    [Google Scholar]
  60. 60.
    Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y et al. 2011. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J. Biol. Chem. 286:5446–54
    [Google Scholar]
  61. 61.
    Oldroyd GE. 2013. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11:252–63
    [Google Scholar]
  62. 62.
    Oyserman BO, Flores SS, Griffioen T, Pan X, van der Wijk E et al. 2022. Disentangling the genetic basis of rhizosphere microbiome assembly in tomato. Nat. Commun. 13:3228Metagenomic data expedited the identification of plant and microbial genes underpinning host–microbiota interactions in wild and domesticated tomato genotypes.
    [Google Scholar]
  63. 63.
    Pankievicz V, Irving TB, Maia LG, Ané J-M. 2019. Are we there yet? The long walk towards the development of efficient symbiotic associations between nitrogen-fixing bacteria and non-leguminous crops. BMC Biol. 17:99
    [Google Scholar]
  64. 64.
    Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6:763–75
    [Google Scholar]
  65. 65.
    Passera A, Follador A, Morandi S, Miotti N, Ghidoli M et al. 2021. Bacterial communities in the embryo of maize landraces: relation with susceptibility to Fusarium ear rot. Microorganisms 9:2388
    [Google Scholar]
  66. 66.
    Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG et al. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. PNAS 110:6548–53
    [Google Scholar]
  67. 67.
    Pérez-Jaramillo JE, Carrión VJ, Bosse M, Ferrão LFV, de Hollander M et al. 2017. Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits. ISME J. 11:2244–57
    [Google Scholar]
  68. 68.
    Pérez-Jaramillo JE, Carrión VJ, de Hollander M, Raaijmakers JM. 2018. The wild side of plant microbiomes. Microbiome 6:143
    [Google Scholar]
  69. 69.
    Pérez-Jaramillo JE, de Hollander M, Ramírez CA, Mendes R, Raaijmakers JM, Carrión VJ. 2019. Deciphering rhizosphere microbiome assembly of wild and modern common bean (Phaseolus vulgaris) in native and agricultural soils from Colombia. Microbiome 7:114
    [Google Scholar]
  70. 70.
    Pérez-Jaramillo JE, Mendes R, Raaijmakers JM. 2016. Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol. Biol. 90:635–44
    [Google Scholar]
  71. 71.
    Polturak G, Dippe M, Stephenson MJ, Chandra Misra R, Owen C et al. 2022. Pathogen-induced biosynthetic pathways encode defense-related molecules in bread wheat. PNAS 119:e2123299119
    [Google Scholar]
  72. 72.
    Purugganan MD, Fuller DQ. 2009. The nature of selection during plant domestication. Nature 457:843–48
    [Google Scholar]
  73. 73.
    Raaijmakers JM, Kiers ET. 2022. Rewilding plant microbiomes. Science 378:599–600
    [Google Scholar]
  74. 74.
    Robertson-Albertyn S, Alegria Terrazas R, Balbirnie K, Blank M, Janiak A et al. 2017. Root hair mutations displace the barley rhizosphere microbiota. Front. Plant Sci. 8:1094
    [Google Scholar]
  75. 75.
    Roman-Reyna V, Pinili D, Borja FN, Quibod IL, Groen SC et al. 2020. Characterization of the leaf microbiome from whole-genome sequencing data of the 3000 Rice Genomes Project. Rice 13:72
    [Google Scholar]
  76. 76.
    Russell J, Mascher M, Dawson IK, Kyriakidis S, Calixto C et al. 2016. Exome sequencing of geographically diverse barley landraces and wild relatives gives insights into environmental adaptation. Nat. Genet. 48:1024–30
    [Google Scholar]
  77. 77.
    Sasaki E, Zhang P, Atwell S, Meng D, Nordborg M. 2015.. “ Missing” G × E variation controls flowering time in Arabidopsis thaliana. PLOS Genet. 11:e1005597
    [Google Scholar]
  78. 78.
    Schlaeppi K, Bulgarelli D. 2015. The plant microbiome at work. Mol. Plant-Microbe Interact. 28:212–17
    [Google Scholar]
  79. 79.
    Schmidt SB, Brown LK, Booth A, Wishart J, Hedley PE et al. 2023. Heritage genetics for adaptation to marginal soils in barley. Trends Plant Sci. 28:5P544–51
    [Google Scholar]
  80. 80.
    Schulthess AW, Kale SM, Liu F, Zhao Y, Philipp N et al. 2022. Genomics-informed prebreeding unlocks the diversity in genebanks for wheat improvement. Nat. Genet. 54:1544–52
    [Google Scholar]
  81. 81.
    Simonin M, Briand M, Chesneau G, Rochefort A, Marais C et al. 2022. Seed microbiota revealed by a large-scale meta-analysis including 50 plant species. New Phytol. 234:1448–63Comprehensive cross-species survey of the seed microbiota.
    [Google Scholar]
  82. 82.
    Subbarao G, Nakahara K, Ishikawa T, Ono H, Yoshida M et al. 2013. Biological nitrification inhibition (BNI) activity in sorghum and its characterization. Plant Soil 366:243–59
    [Google Scholar]
  83. 83.
    Tan X, Xie H, Yu J, Wang Y, Xu J et al. 2022. Host genetic determinants drive compartment-specific assembly of tea plant microbiomes. Plant Biotechnol. J. 20:112174–86
    [Google Scholar]
  84. 84.
    Terrazas RA, Giles C, Paterson E, Robertson-Albertyn S, Cesco S et al. 2016. Plant–microbiota interactions as a driver of the mineral turnover in the rhizosphere. Adv. Appl. Microbiol. 95:1–67
    [Google Scholar]
  85. 85.
    Theis KR, Dheilly NM, Klassen JL, Brucker RM, Baines JF et al. 2016. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1:e00028–16
    [Google Scholar]
  86. 86.
    Truyens S, Weyens N, Cuypers A, Vangronsveld J. 2015. Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ. Microbiol. Rep. 7:40–50
    [Google Scholar]
  87. 87.
    Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M et al. 2013. Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J. 7:2248–58
    [Google Scholar]
  88. 88.
    Van Deynze A, Zamora P, Delaux P-M, Heitmann C, Jayaraman D et al. 2018. Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota. PLOS Biol. 16:e2006352Example of plant organ specialization (i.e., mucilage-producing aerial roots) supporting nitrogen-fixing bacteria in maize.
    [Google Scholar]
  89. 89.
    VanWallendael A, Benucci GMN, da Costa PB, Fraser L, Sreedasyam A et al. 2022. Host genotype controls ecological change in the leaf fungal microbiome. PLOS Biol. 20:e3001681
    [Google Scholar]
  90. 90.
    Vorholt JA, Vogel C, Carlström CI, Müller DB. 2017. Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host Microbe 22:142–55
    [Google Scholar]
  91. 91.
    Wagner MR. 2021. Prioritizing host phenotype to understand microbiome heritability in plants. New Phytol. 232:502–9
    [Google Scholar]
  92. 92.
    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 Phytol. 225:2152–65
    [Google Scholar]
  93. 93.
    Wagner MR, Tang C, Salvato F, Clouse KM, Bartlett A et al. 2021. Microbe-dependent heterosis in maize. PNAS 118:e2021965118First demonstration of microbiota contribution to plant heterosis.
    [Google Scholar]
  94. 94.
    Wallace JG, Kremling KA, Kovar LL, Buckler ES. 2018. Quantitative genetics of the maize leaf microbiome. Phytobiomes J. 2:208–24
    [Google Scholar]
  95. 95.
    Walters WA, Jin Z, Youngblut N, Wallace JG, Sutter J et al. 2018. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. PNAS 115:7368–73
    [Google Scholar]
  96. 96.
    Wang P, Chai YN, Roston R, Dayan FE, Schachtman DP. 2021. The sorghum bicolor root exudate sorgoleone shapes bacterial communities and delays network formation. mSystems 6:e00749–20
    [Google Scholar]
  97. 97.
    Wang Y, Wang X, Sun S, Jin C, Su J et al. 2022. GWAS, MWAS and mGWAS provide insights into precision agriculture based on genotype-dependent microbial effects in foxtail millet. Nat. Commun. 13:5913Establishment of a causal relationship between microbiota recruitment and plant performance in crops.
    [Google Scholar]
  98. 98.
    Watson A, Ghosh S, Williams MJ, Cuddy WS, Simmonds J et al. 2018. Speed breeding is a powerful tool to accelerate crop research and breeding. Nat. Plants 4:23–29
    [Google Scholar]
  99. 99.
    Wille L, Kurmann M, Messmer MM, Studer B, Hohmann P. 2021. Untangling the pea root rot complex reveals microbial markers for plant health. Front. Plant Sci. 12:737820
    [Google Scholar]
  100. 100.
    Wille L, Messmer MM, Studer B, Hohmann P. 2019. Insights to plant–microbe interactions provide opportunities to improve resistance breeding against root diseases in grain legumes. Plant Cell Environ. 42:20–40
    [Google Scholar]
  101. 101.
    Wipf HM, Coleman-Derr D. 2021. Evaluating domestication and ploidy effects on the assembly of the wheat bacterial microbiome. PLOS ONE 16:e0248030
    [Google Scholar]
  102. 102.
    Wissuwa M, Mazzola M, Picard C. 2009. Novel approaches in plant breeding for rhizosphere-related traits. Plant Soil 321:409–30
    [Google Scholar]
  103. 103.
    Wouters FC, Blanchette B, Gershenzon J, Vassão DG. 2016. Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores. Phytochem. Rev. 15:1127–51
    [Google Scholar]
  104. 104.
    Xu L, Dong Z, Chiniquy D, Pierroz G, Deng S et al. 2021. Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics. Nat. Commun. 12:3209
    [Google Scholar]
  105. 105.
    Xu L, Naylor D, Dong Z, Simmons T, Pierroz G et al. 2018. Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. PNAS 115:E4284–93
    [Google Scholar]
  106. 106.
    Yu G, Matny O, Champouret N, Steuernagel B, Moscou MJ et al. 2022. Aegilops sharonensis genome-assisted identification of stem rust resistance gene Sr62. Nat. Commun. 13:1607
    [Google Scholar]
  107. 107.
    Yu H, Li J. 2022. Breeding future crops to feed the world through de novo domestication. Nat. Commun. 13:1171
    [Google Scholar]
  108. 108.
    Yu P, He X, Baer M, Beirinckx S, Tian T et al. 2021. Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation. Nat. Plants 7:481–99
    [Google Scholar]
  109. 109.
    Yu X, Li X, Guo T, Zhu C, Wu Y et al. 2016. Genomic prediction contributing to a promising global strategy to turbocharge gene banks. Nat. Plants 2:16150
    [Google Scholar]
  110. 110.
    Zachow C, Müller H, Tilcher R, Berg G. 2014. Differences between the rhizosphere microbiome of Beta vulgaris ssp. maritima—ancestor of all beet crops—and modern sugar beets. Front. Microbiol. 5:415
    [Google Scholar]
  111. 111.
    Zanini SF, Bayer PE, Wells R, Snowdon RJ, Batley J et al. 2022. Pangenomics in crop improvement—from coding structural variations to finding regulatory variants with pangenome graphs. Plant Genome 15:e20177
    [Google Scholar]
  112. 112.
    Zhang D, Yang K, Kan Z, Dang H, Feng S et al. 2021. The regulatory module MdBT2–MdMYB88/MdMYB124–MdNRTs regulates nitrogen usage in apple. Plant Physiol. 185:1924–42
    [Google Scholar]
  113. 113.
    Zhang J, Liu Y-X, Zhang N, Hu B, Jin T et al. 2019. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat. Biotechnol. 37:676–84Compelling example of how breeding selection impacted microbiota recruitment in rice.
    [Google Scholar]
  114. 114.
    Zhong Y, Xun W, Wang X, Tian S, Zhang Y et al. 2022. Root-secreted bitter triterpene modulates the rhizosphere microbiota to improve plant fitness. Nat. Plants 8:887–96
    [Google Scholar]
  115. 115.
    Zsögön A, Čermák T, Naves ER, Notini MM, Edel KH et al. 2018. De novo domestication of wild tomato using genome editing. Nat. Biotechnol. 36:1211–16
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-021621-121447
Loading
/content/journals/10.1146/annurev-phyto-021621-121447
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error