Crop domestication and improvement reshape root traits and the structure and function of their associated microbiome
Xiaoming HE, Frank HOCHHOLDINGER, Xingping CHEN, Peng YU
Crop domestication and improvement reshape root traits and the structure and function of their associated microbiome
● Crop domestication decreased crop genetic diversity while increasing the complexity of root traits and simplifying the structure and function of their microbiome. | |
● Modern crops have a great genetic potential for manipulating root traits and associated functional microbiome communities. | |
● Exploitation of crop domestication strengthens future crop root systems and microbiome resilience. |
Beneficial root-microbiome interactions offer enormous potential to improve crop performance and stress tolerance. Domestication and improvement reduced the genetic diversity of crops and reshaped their phenotypic traits and their associated microbiome structure and function. However, understanding of the genetic and physiological mechanisms how domestication and improvement modulated root function, microbiome assembly and even co-selective patterns remains largely elusive. This review summarizes the current status of how crop domestication and improvement (heterosis) affected root characteristics and their associated microbiome structure and function. Also, it assesses potential mechanisms how crop domestication and improvement reshaped root-microbiome association through gene regulation, root structure and function and root exudate features. A hypothetical strategy is proposed that entangles crop genetics and abiotic interactions with beneficial microbiomes to mitigate the effects of global climate change on crop performance. A comprehensive understanding of the role of crop domestication and improvement in root-associated microbiome interaction will advance future breeding efforts and agricultural management.
Crop domestication / heterosis / micro-biome / root development / exploitation strategy
[1] |
Zhang M Y, Kong X P . How plants discern friends from foes. Trends in Plant Science, 2022, 27(2): 107–109
CrossRef
Google scholar
|
[2] |
Yu P, He X M, Baer M, Beirinckx S, Tian T, Moya Y A T, Zhang X C, Deichmann M, Frey F P, Bresgen V, Li C J, Razavi B S, Schaaf G, Von Wirén N, Su Z, Bucher M, Tsuda K, Goormachtig S, Chen X P, Hochholdinger F . Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation. Nature Plants, 2021, 7(4): 481–499
CrossRef
Google scholar
|
[3] |
Oldroyd G E D, Leyser O . A plant’s diet, surviving in a variable nutrient environment. Science, 2020, 368(6486): eaba0196
CrossRef
Google scholar
|
[4] |
Favela A O, Bohn M D, Kent A . Maize germplasm chronosequence shows crop breeding history impacts recruitment of the rhizosphere microbiome. ISME Journal, 2021, 15(8): 2454–2464
CrossRef
Google scholar
|
[5] |
Kim H, Lee K K, Jeon J, Harris W A, Lee Y H . Domestication of Oryza species eco-evolutionarily shapes bacterial and fungal communities in rice seed. Microbiome, 2020, 8(1): 20
CrossRef
Google scholar
|
[6] |
Pérez-Jaramillo J E, Carrión V J, Bosse M, Ferrao L F V, de Hollander M, Garcia A A F, Ramírez C A, Mendes R, Raaijmakers J M . Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits. ISME Journal, 2017, 11(10): 2244–2257
CrossRef
Google scholar
|
[7] |
Galindo-Castañeda T, Hartmann M, Lynch J P . Location: root architecture structures rhizosphere microbial associations. Journal of Experimental Botany, 2024, 75(2): 594–604
CrossRef
Google scholar
|
[8] |
Cheng Y T, Zhang L, He S Y . Plant–microbe interactions facing environmental challenge. Cell Host & Microbe, 2019, 26(2): 183–192
CrossRef
Google scholar
|
[9] |
Rudgers J A, Afkhami M E, Bell-Dereske L, Chung Y A, Crawford K M, Kivlin S N, Mann M A, Nuñez M A . Climate disruption of plant-microbe interactions. Annual Review of Ecology, Evolution, and Systematics, 2020, 51(1): 561–586
CrossRef
Google scholar
|
[10] |
de Vries F T, Griffiths R I, Knight C G, Nicolitch O, Williams A . Harnessing rhizosphere microbiomes for drought-resilient crop production. Science, 2020, 368(6488): 270–274
CrossRef
Google scholar
|
[11] |
He X, Wang D, Jiang Y, Li M, Delgado-Baquerizo M, Mclaughlin C, Marcon C, Guo L, Baer M, Moya Y A T, von Wirén N, Deichmann M, Schaaf G, Piepho H P, Yang Z, Yang J, Yim B, Smalla K, Goormachtig S, de Vries F T, Hüging H, Baer M, Sawers R J H, Reif J C, Hochholdinger F, Chen X, Yu P . Heritable microbiome variation is correlated with source environment in locally adapted maize varieties. Nature Plants, 2024, 10(4): 598–617
CrossRef
Google scholar
|
[12] |
Baldauf J A, Hochholdinger F . Molecular dissection of heterosis in cereal roots and their rhizosphere. Theoretical and Applied Genetics, 2023, 136(8): 173
CrossRef
Google scholar
|
[13] |
Yamasaki M, Tenaillon M I, Vroh Bi I, Schroeder S G, Sanchez-Villeda H, Doebley J F, Gaut B S, Mcmullen M D . A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement. Plant Cell, 2005, 17(11): 2859–2872
CrossRef
Google scholar
|
[14] |
Yue H, Yue W J, Jiao S, Kim H, Lee Y H, Wei G H, Song W N, Shu D T . Plant domestication shapes rhizosphere microbiome assembly and metabolic functions. Microbiome, 2023, 11(1): 70
CrossRef
Google scholar
|
[15] |
Raaijmakers J M, Kiers E T . Rewilding plant microbiomes. Science, 2022, 378(6620): 599–600
CrossRef
Google scholar
|
[16] |
Schmidt J E, Mazza Rodrigues J L, Brisson V L, Kent A, Gaudin A C M . Impacts of directed evolution and soil management legacy on the maize rhizobiome. Soil Biology & Biochemistry, 2020, 145: 107794
CrossRef
Google scholar
|
[17] |
Brisson V L, Schmidt J E, Northen T R, Vogel J P, Gaudin A C M . Impacts of maize domestication and breeding on rhizosphere microbial community recruitment from a nutrient depleted agricultural soil. Scientific Reports, 2019, 9(1): 15611
CrossRef
Google scholar
|
[18] |
Pérez-Jaramillo J E, Carrión V J, de Hollander M, Raaijmakers J M . The wild side of plant microbiomes. Microbiome, 2018, 6(1): 143
CrossRef
Google scholar
|
[19] |
Xiong C, Zhu Y G, Wang J T, Singh B, Han L L, Shen J P, Li P P, Wang G B, Wu C F, Ge A H, Zhang L M, He J Z . Host selection shapes crop microbiome assembly and network complexity. New Phytologist, 2021, 229(2): 1091–1104
CrossRef
Google scholar
|
[20] |
Walters W A, Jin Z, Youngblut N, Wallace J G, Sutter J, Zhang W, González-Peña A, Peiffer J, Koren O, Shi Q J, Knight R, Glavina del Rio T, Tringe S G, Buckler E S, Dangl J L, Ley R E . Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(28): 7368–7373
CrossRef
Google scholar
|
[21] |
Wagner M R, Roberts J H, Balint-Kurti P, Holland J B . Heterosis of leaf and rhizosphere microbiomes in field-grown maize. New Phytologist, 2020, 228(3): 1055–1069
CrossRef
Google scholar
|
[22] |
Leff J W, Lynch R C, Kane N C, Fierer N . Plant domestication and the assembly of bacterial and fungal communities associated with strains of the common sunflower. Helianthus annuus. New Phytologist, 2017, 214(1): 412–423
CrossRef
Google scholar
|
[23] |
Yu P, Li C, Li M, He X, Wang D, Li H, Marcon C, Li Y, Perez-Limón S, Chen X, Delgado-Baquerizo M, Koller R, Metzner R, van Dusschoten D, Pflugfelder D, Borisjuk L, Plutenko I, Mahon A, Resende M F R Jr, Salvi S, Akale A, Abdalla M, Ahmed M A, Bauer F M, Schnepf A, Lobet G, Heymans A, Suresh K, Schreiber L, McLaughlin C M, Li C, Mayer M, Schön C C, Bernau V, von Wirén N, Sawers R J H, Wang T, Hochholdinger F . Seedling root system adaptation to water availability during maize domestication and global expansion. Nature Genetics, 2024, 56(6): 1245–1256
CrossRef
Google scholar
|
[24] |
Burton A L, Brown K M, Lynch J P . Phenotypic diversity of root anatomical and architectural traits in Zea species. Crop Science, 2013, 53(3): 1042–1055
CrossRef
Google scholar
|
[25] |
Isaac M E, Nimmo V, Gaudin A C M, Leptin A, Schmidt J E, Kallenbach C M, Martin A, Entz M, Carkner M, Rajcan I, Boyle T D, Lu X . Crop domestication, root trait syndromes, and soil nutrient acquisition in organic agroecosystems: a systematic review. Frontiers in Sustainable Food Systems, 2021, 5: 716480
CrossRef
Google scholar
|
[26] |
Li Y, Chen H, Gu L, Wu J, Zheng X, Fan Z, Pan D, Li J T, Shu W, Rosendahl S, Wang Y . Domestication of rice may have changed its arbuscular mycorrhizal properties by modifying phosphorus nutrition-related traits and decreasing symbiotic compatibility. New Phytologist, 2024, 243(4): 1554–1570
CrossRef
Google scholar
|
[27] |
Wei H Y, Hu L, Zhu Y, Xu D, Zheng L M, Chen Z F, Hu Y J, Cui P Y, Guo B W, Dai Q G, Zhang H C . Different characteristics of nutrient absorption and utilization between inbred japonica super rice and inter-sub-specific hybrid super rice. Field Crops Research, 2018, 218: 88–96
CrossRef
Google scholar
|
[28] |
Martín-Robles N, Lehmann A, Seco E, Aroca R, Rillig M C, Milla R . Impacts of domestication on the arbuscular mycorrhizal symbiosis of 27 crop species. New Phytologist, 2018, 218(1): 322–334
CrossRef
Google scholar
|
[29] |
Iannucci A, Fragasso M, Beleggia R, Nigro F, Papa R . Evolution of the crop rhizosphere: Impact of domestication on root exudates in tetraploid wheat (Triticum turgidum L.). Frontiers in Plant Science, 2017, 8: 2124
CrossRef
Google scholar
|
[30] |
Picard C, Bosco M . Maize heterosis affects the structure and dynamics of indigenous rhizospheric auxins-producing Pseudomonas populations. FEMS Microbiology Ecology, 2005, 53(3): 349–357
CrossRef
Google scholar
|
[31] |
Hoecker N, Keller B, Piepho H P, Hochholdinger F . Manifestation of heterosis during early maize (Zea mays L.) root development. Theoretical and Applied Genetics, 2006, 112(3): 421–429
CrossRef
Google scholar
|
[32] |
Picard C, Baruffa E, Bosco M . Enrichment and diversity of plant-probiotic microorganisms in the rhizosphere of hybrid maize during four growth cycles. Soil Biology & Biochemistry, 2008, 40(1): 106–115
CrossRef
Google scholar
|
[33] |
An G H, Kobayashi S, Enoki H, Sonobe K, Muraki M, Karasawa T, Ezawa T . How does arbuscular mycorrhizal colonization vary with host plant genotype? An example based on maize (Zea mays) germplasms. Plant and Soil, 2010, 327(1−2): 441–453
CrossRef
Google scholar
|
[34] |
Szoboszlay M, Lambers J, Chappell J, Kupper J V, Moe L A, Mcnear D H Jr . Comparison of root system architecture and rhizosphere microbial communities of Balsas teosinte and domesticated corn cultivars. Soil Biology & Biochemistry, 2015, 80: 34–44
CrossRef
Google scholar
|
[35] |
Spor A, Roucou A, Mounier A, Bru D, Breuil M C, Fort F, Vile D, Roumet P, Philippot L, Violle C . Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat. Scientific Reports, 2020, 10(1): 12234
CrossRef
Google scholar
|
[36] |
Alegria Terrazas R, Balbirnie-Cumming K, Morris J, Hedley P E, Russell J, Paterson E, Baggs E M, Fridman E, Bulgarelli D . A footprint of plant eco-geographic adaptation on the composition of the barley rhizosphere bacterial microbiota. Scientific Reports, 2020, 10(1): 12916
CrossRef
Google scholar
|
[37] |
Lopez-Valdivia I, Perkins A C, Schneider H M, Vallebueno-Estrada M, Burridge J D, Gonzalez-Orozco E, Montufar A, Montiel R, Lynch J P, Vielle-Calzada J P . Gradual domestication of root traits in the earliest maize from Tehuacan. Proceedings of the National Academy of Sciences of the United States of America, 2022, 119(17): e2110245119
CrossRef
Google scholar
|
[38] |
Gaudin A C M, Mcclymont S A, Soliman S S M, Raizada M N . The effect of altered dosage of a mutant allele of Teosinte branched 1 (tb1-ref) on the root system of modern maize. BMC Genetics, 2014, 15(1): 23
CrossRef
Google scholar
|
[39] |
Wild A J, Steiner F A, Kiene M, Tyborski N, Tung S Y, Koehler T, Carminati A, Eder B, Groth J, Vahl W K, Wolfrum S, Lueders T, Laforsch C, Mueller C W, Vidal A, Pausch J . Unraveling root and rhizosphere traits in temperate maize landraces and modern cultivars: Implications for soil resource acquisition and drought adaptation. Plant, Cell & Environment, 2024, 47(7): 2524–2539
CrossRef
Google scholar
|
[40] |
Cotton T E A, Pétriacq P, Cameron D D, Meselmani M A, Schwarzenbacher R, Rolfe S A, Ton J . Metabolic regulation of the maize rhizobiome by benzoxazinoids. ISME Journal, 2019, 13(7): 1647–1658
CrossRef
Google scholar
|
[41] |
Xu G H, Cao J J, Wang X F, Chen Q Y, Jin W W, Li Z, Tian F . Evolutionary metabolomics identifies substantial metabolic divergence between maize and its wild ancestor, teosinte. Plant Cell, 2019, 31(9): 1990–2009
CrossRef
Google scholar
|
[42] |
Ben-Abu Y, Itsko M . Metabolome dynamics during wheat domestication. Scientific Reports, 2022, 12(1): 8532
CrossRef
Google scholar
|
[43] |
Baldauf J A, Marcon C, Lithio A, Vedder L, Altrogge L, Piepho H P, Schoof H, Nettleton D, Hochholdinger F . Single-parent expression is a general mechanism driving extensive complementation of non-syntenic genes in maize hybrids. Current Biology, 2018, 28(3): 431–437
CrossRef
Google scholar
|
[44] |
Hochholdinger F, Baldauf J A . Heterosis in plants. Current Biology, 2018, 28(18): R1089–R1092
CrossRef
Google scholar
|
[45] |
Hochholdinger F, Hoecker N . Towards the molecular basis of heterosis. Trends in Plant Science, 2007, 12(9): 427–432
CrossRef
Google scholar
|
[46] |
Liu Y H, Zhao K K, Stirling E, Wang X L, Gao Z Y, Ma B, Xu C M, Chen S, Chu G, Zhang X F, Wang D Y . Heterosis of endophytic microbiomes in hybrid rice varieties improves seed germination. mSystems, 2024, 9(5): e0000424
CrossRef
Google scholar
|
[47] |
Zhang M, Wang Y, Hu Y, Wang H, Liu Y, Zhao B, Zhang J, Fang R, Yan Y . Heterosis in root microbiota inhibits growth of soil-borne fungal pathogens in hybrid rice. Journal of Integrative Plant Biology, 2023, 65(4): 1059–1076
CrossRef
Google scholar
|
[48] |
Wagner M R, Tang C, Salvato F, Clouse K M, Bartlett A, Vintila S, Phillips L, Sermons S, Hoffmann M, Balint-Kurti P J, Kleiner M . Microbe-dependent heterosis in maize. Proceedings of the National Academy of Sciences of the United States of America, 2021, 118(30): e2021965118
CrossRef
Google scholar
|
[49] |
Tian L, Wang E Z, Lin X L, Ji L, Chang J J, Chen H P, Wang J L, Chen D Z, Tran L S P, Tian C J . Wild rice harbors more root endophytic fungi than cultivated rice in the F1 offspring after crossbreeding. BMC Genomics, 2021, 22(1): 278
CrossRef
Google scholar
|
[50] |
Gomes E A, Lana U G P, Quensen J F, De Sousa S M, Oliveira C A, Guo J R, Guimaraes L J M, Tiedje J M . Root-associated nicrobiome of maize genotypes with contrasting phosphorus use efficiency. Phytobiomes Journal, 2018, 2(3): 129–137
CrossRef
Google scholar
|
[51] |
Wang Z K, Ni Z F, Wu H L, Nie X L, Sun Q X . Heterosis in root development and differential gene expression between hybrids and their parental inbreds in wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 2006, 113(7): 1283–1294
CrossRef
Google scholar
|
[52] |
Sharma S, Demason D A, Ehdaie B, Lukaszewski A J, Waines J G . Dosage effect of the short arm of chromosome 1 of rye on root morphology and anatomy in bread wheat. Journal of Experimental Botany, 2010, 61(10): 2623–2633
CrossRef
Google scholar
|
[53] |
Zhai R R, Feng Y, Wang H M, Zhan X D, Shen X H, Wu W M, Zhang Y X, Chen D B, Dai G X, Yang Z L, Cao L Y, Cheng S H . Transcriptome analysis of rice root heterosis by RNA-Seq. BMC Genomics, 2013, 14(1): 19
CrossRef
Google scholar
|
[54] |
Paschold A, Marcon C, Hoecker N, Hochholdinger F . Molecular dissection of heterosis manifestation during early maize root development. Theoretical and Applied Genetics, 2010, 120(2): 383–388
CrossRef
Google scholar
|
[55] |
Cavani L, Mimmo T . Rhizodeposition of Zea mays L. as affected by heterosis. Archives of Agronomy and Soil Science, 2007, 53(6): 593–604
CrossRef
Google scholar
|
[56] |
Meyer R S, Purugganan M D . Evolution of crop species: genetics of domestication and diversification. Nature Reviews. Genetics, 2013, 14(12): 840–852
CrossRef
Google scholar
|
[57] |
Van Deynze A, Zamora P, Delaux P M, Heitmann C, Jayaraman D, Rajasekar S, Graham D, Maeda J, Gibson D, Schwartz K D, Berry A M, Bhatnagar S, Jospin G, Darling A, Jeannotte R, Lopez J, Weimer B C, Eisen J A, Shapiro H Y, Ané J M, Bennett A B . Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota. PLoS Biology, 2018, 16(8): e2006352
CrossRef
Google scholar
|
[58] |
Pattnaik D, Avinash S P, Panda S, Bansal K C, Chakraborti M, Kar M K, Baig M J, Molla K A . Accelerating crop domestication through genome editing for sustainable agriculture. Journal of Plant Biochemistry and Biotechnology, 2023, 32(4): 688–704
CrossRef
Google scholar
|
[59] |
Shen J Y, Wang M X, Wang E T . Exploitation of the microbiome for crop breeding. Nature Plants, 2024, 10(4): 533–534
CrossRef
Google scholar
|
[60] |
Sawers R J H, Ramírez-Flores M R, Olalde-Portugal V, Paszkowski U . The impact of domestication and crop improvement on arbuscular mycorrhizal symbiosis in cereals: insights from genetics and genomics. New Phytologist, 2018, 220(4): 1135–1140
CrossRef
Google scholar
|
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