| BMC Genetics | |
| The effect of altered dosage of a mutant allele of Teosinte branched 1 (tb1-ref) on the root system of modern maize | |
| Manish N Raizada1  Sameh SM Soliman1  Sarah A McClymont1  Amelie CM Gaudin1  | |
| [1] Department of Plant Agriculture, University of Guelph, 50 Stone Road, Guelph, Ontario N1G 2W1, Canada | |
| 关键词: Crown root; Lateral root; Architecture; Root; Tiller; Tb1; Teosinte branched 1; Teosinte; Domestication; Zea; Maize; | |
| Others : 1085797 DOI : 10.1186/1471-2156-15-23 |
|
| received in 2013-10-09, accepted in 2014-02-06, 发布年份 2014 | |
PDF
|
|
【 摘 要 】
Background
There was ancient human selection on the wild progenitor of modern maize, Balsas teosinte, for decreased shoot branching (tillering), in order to allow more nutrients to be diverted to grain. Mechanistically, the decline in shoot tillering has been associated with selection for increased expression of the major domestication gene Teosinte Branched 1 (Tb1) in shoot primordia. Therefore, TB1 has been defined as a repressor of shoot branching. It is known that plants respond to changes in shoot size by compensatory changes in root growth and architecture. However, it has not been reported whether altered TB1 expression affects any plant traits below ground. Previously, changes in dosage of a well-studied mutant allele of Tb1 in modern maize, called tb1-ref, from one to two copies, was shown to increase tillering. As a result, plants with two copies of the tb1-ref allele have a larger shoot biomass than heterozygotes. Here we used aeroponics to phenotype the effects of tb1-ref copy number on maize roots at macro-, meso- and micro scales of development.
Results
An increase in the tb1-ref copy number from one to two copies resulted in: (1) an increase in crown root number due to the cumulative initiation of crown roots from successive tillers; (2) higher density of first and second order lateral roots; and (3) reduced average lateral root length. The resulting increase in root system biomass in homozygous tb1-ref mutants balanced the increase in shoot biomass caused by enhanced tillering. These changes caused homozygous tb1-ref mutants of modern maize to more closely resemble its ancestor Balsas teosinte below ground.
Conclusion
We conclude that a decrease in TB1 function in maize results in a larger root system, due to an increase in the number of crown roots and lateral roots. Given that decreased TB1 expression results in a more highly branched and larger shoot, the impact of TB1 below ground may be direct or indirect. We discuss the potential implications of these findings for whole plant coordination of biomass accumulation and maize domestication.
【 授权许可】
2014 Gaudin et al.; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
|---|---|---|---|
| 20150113180544402.pdf | 3071KB | ||
| Figure 7. | 28KB | Image | |
| Figure 6. | 78KB | Image | |
| Figure 5. | 34KB | Image | |
| Figure 4. | 78KB | Image | |
| Figure 3. | 124KB | Image | |
| Figure 2. | 185KB | Image | |
| Figure 1. | 136KB | Image |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
【 参考文献 】
- [1]Doebley J: Molecular evidence and the evolution of maize. Econ Bot 1990, 44:6-27.
- [2]Ranere AJ, Piperno DR, Holst I, Dickau R, Iriarte J: The cultural and chronological context of early Holocene maize and squash domestication in the Central Balsas River Valley, Mexico. Proc Natl Acad Sci USA 2009, 106:5014-5018.
- [3]Piperno DR, Ranere AJ, Holst I, Iriarte J, Dickau R: Starch grain and phytolith evidence for early ninth millennium B.P. maize from the Central Balsas River Valley, Mexico. Proc Natl Acad Sci USA 2009, 106:5019-5024.
- [4]Hastorf CA: Rio Balsas most likely region for maize domestication. Proc Natl Acad Sci USA 2009, 106:4957-4958.
- [5]Sluyter A, Dominquez G: Early maize (Zea mays L.) cultivation in Mexico: dating sedimentary pollen records and its implications. Proc Natl Acad Sci USA 2006, 103:1147-1151.
- [6]Fukunaga K, Hill J, Vigouroux Y, Matsuoka Y, Sanchez GJ, Lui K, Buckler ES, Doebley J: Genetic diversity and population structure of teosinte. Genetics 2005, 169:2241-2254.
- [7]Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler E, Doebley J: A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 2002, 99:6080-6084.
- [8]Purugganan MD, Fuller DQ: The nature of selection during plant domestication. Nature 2009, 457:843-848.
- [9]Doebley J, Gaut BS, Smith BD: The molecular genetics of crop domestication. Cell 2006, 127:1309-1321.
- [10]Doebley J, Stec A, Gustus C: Teosinte Branched1 and the origin of maize: Evidence for epistasis and the evolution of dominance. Genetics 1995, 141:333-346.
- [11]Doebley J, Stec A, Hubbard L: The evolution of apical dominance in maize. Nature 1997, 386:485-488.
- [12]Doebley J: The genetics of maize evolution. Ann Rev Genet 2004, 38:37-59.
- [13]Lukens L, Doebley J: Molecular evolution of the Teosinte Branched gene among maize and related grasses. Mol Biol Evol 2001, 18:627-638.
- [14]Cubas P, Lauter N, Doebley J, Coen E: The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 1999, 18:215-222.
- [15]Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P: Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA 2005, 102:12978-12983.
- [16]Kosugi S, Ohashi Y: DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 2002, 30:337-348.
- [17]Hubbard L, McSteen P, Doebley J, Hake S: Expression patterns and mutant phenotype of Teosinte Branched1 correlate with growth suppression in maize and teosinte. Genetics 2002, 162:1927-1935.
- [18]Clark RM, Wagler TN, Quijada P, Doebley J: A distant upstream enhancer at the maize domestication gene Tb1 has pleiotropic effects on plant and inflorescent architecture. Nat Genet 2006, 38:594-597.
- [19]Zhao Q, Thuillet A-C, Uhlmann NK, Weber A, Rafalski JA, Allen SM, Tingley S, Doebley J: The role of regulatory genes during maize domestication: evidence from nucleotide polymorphism and gene expression. Genetics 2008, 178:2133-2143.
- [20]Studer A, Zhao Q, Ross-Ibarra J, Doebley J: Identification of a functional transposon insertion in the maize domestication gene Tb1. Nat Genet 2011, 43:1160-1163.
- [21]Zhou LL, Zhang JY, Yan JB, Song RT: Two transposable element insertions are causative mutations for the major domestication gene Teosinte Branched 1 in modern maize. Cell Res 2011, 21:1267-1270.
- [22]Gaudin ACM, McClymont SA, Holmes BM, Lyons E, Raizada MN: Novel temporal, fine-scale and growth variation phenotypes in roots of adult-stage maize (Zea mays L.) in response to low nitrogen stress. Plant Cell Environ 2011, 34:2122-2137.
- [23]Hochholdinger F, Woll K, Sauer M, Dembinsky D: Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann Bot 2004, 93:359-368.
- [24]Gaudin ACM, McClymont SA, Raizada MN: The nitrogen adaptation strategy of the wild teosinte ancestor of modern maize, Zea mays subsp. parviglumis. Crop Sci 2011, 51:2780-2795.
- [25]Burnham C: Teosinte branched. Maize Genet Coop Newslett 1959, 33:74.
- [26]Waisel Y: Aeroponics: a tool for root research. In Plant Roots: The Hidden Half. Edited by Waisel Y, Eshel A, Kafkafi U. New York: Marcel Dekker Inc; 1996:239-245.
- [27]Kratsch HA, Graves WR, Gladon RJ: Aeroponic system for control of root-zone atmosphere. Environ Expt Bot 2006, 55:70-76.
- [28]Gilroy S, Jones DL: Through form to function: root hair development and nutrient uptake. Trends Plant Sci 2000, 5:56-60.
- [29]Finlayson SA: Arabidopsis TEOSINTE BRANCHED1-LIKE 1 regulates axillary bud outgrowth and is homologous to monocot TEOSINTE BRANCHED1. Plant Cell Physiol 2007, 48:667-677.
- [30]Kebrom TH, Brutnell TP, Finlayson SA: Suppression of sorghum axillary bud outgrowth by shade, phyB and defoliation signalling pathways. Plant Cell Environ 2009, 33:48-58.
- [31]Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C: The OsTB1 gene negatively regulates lateral branching in rice. Plant J 2003, 33:513-520.
- [32]Lewis J, Mackintosh C, Shin S, Gilding E, Kravchenko S, Baldridge G, Zeyen R, Muehlbauer GJ: Overexpression of the maize Teosinte Branched1 gene in wheat suppresses tiller development. Plant Cell Rep 2008, 27:1217-1225.
- [33]Ramsay L, Comadran J, Druka A, Marshall DF, Thomas WT, Macaulay M, MacKenzie K, Simpson C, Fuller J, Bonar N, Hayes PM, Lundqvist U, Franckowiak JD, Close TJ, Muehlbauer GJ, Waugh R: INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1. Nat Genet 2011, 43:169-172.
- [34]Roycewicz P, Malamy JE: Dissecting the effects of nitrate, sucrose and osmotic potential on Arabidopsis root and shoot system growth in laboratory assays. Philos Trans R Soc Lond B Biol Sci 2012, 367:1489-1500.
- [35]Wacker L, Jacomet S, Körner C: Trends in biomass fractionation in wheat and barley from wild ancestors to modern cultivars. Plant Biol 2002, 4:258-265.
- [36]Demotes-Mainard S, Pellerin S: Effect of mutual shading on the emergence of nodal roots and the root/shoot ratio of maize. Plant Soil 1992, 147:87-93.
- [37]Hebert Y, Guingo E, Loudet O: The response of root/shoot partitioning and root morphology to light reduction in maize genotypes. Crop Sci 2001, 41:363-371.
- [38]Xu M, Zhu L, Shou H, Wu P: A PIN1 Family Gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 2005, 46:1674-1681.
- [39]Kebrom TH, Brutnell TP: The molecular analysis of the shade avoidance syndrome in the grasses has begun. J Exp Bot 2007, 58:3079-3089.
- [40]Hockett EA: Relationship of adventitious roots and agronomic characteristics in barley. Can J Plant Sci 1986, 66:257-266.
- [41]Lo S-F, Yang S-Y, Chen K-T, Hsing Y-I, Zeevaart JAD, Chen LJ, Yu SM: A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 2008, 20:2603-2618.
- [42]MacKey J: Wheat domestication as shoot: root interrelation process. In Proceedings Fifth International Wheat Genetics Symposium: 27-30 June 1978. Edited by Ramanujam S. New Delhi: Indian Agricultural Research Institute; 1978:875-890.
- [43]Anderson-Taylor G, Marshall C: Root-tiller interrelationships in spring barley. Ann Bot 1983, 51:47-58.
- [44]Chloupek O, Forster B, Thomas W: The effect of semi-dwarf genes on root system size in field-grown barley. Theor Appl Genet 2006, 112:779-786.
- [45]Kasperbauer MJ, Karlen DL: Light-mediated bioregulation of tillering and photosynthate partitioning in wheat. Physiol Planta 1986, 66:159-163.
- [46]Sparkes DL, Berry P, King M: Effects of shade on root characters associated with lodging in wheat (Triticum aestivum). Ann Appl Biol 2008, 152:389-395.
- [47]Simons JL, Napoli CA, Janssen BJ, Plummer KM, Snowden KC: Analysis of the DECREASED APICAL DOMINANCE genes of petunia in the control of axillary branching. Plant Physiol 2007, 143:697-706.
- [48]Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ: The decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 2005, 17:746-759.
- [49]Robertson BM, Waines JG, Gill BS: Genetic variability for seedling root numbers in wild and domesticated wheats. Crop Sci 1979, 19:843-847.
- [50]Grando S, Ceccarelli S: Seminal root morphology and coleoptile length in wild (Hordeum vulgare ssp. spontaneum) and cultivated (Hordeum vulgare ssp. vulgare) barley. Euphytica 1995, 86:73-80.
- [51]Gordon DC, Bengough AG, Clark S, Al-Meanaie HS, Thomas WTB, Forster BP: A phenotypic screen for genetic analysis of barley seedling root traits. Aspect Appl Biol 2005, 73:81-84.
- [52]Beeckman T, Burssens S, Inze D: The peri-cell-cycle in Arabidopsis. J Expt Bot 2001, 52:403-411.
- [53]Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inze D, Beeckman T: Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 2002, 14:2339-2351.
- [54]Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml JA, Shishkova S, Celenza J, Benková E: Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 2008, 105:8790-8794.
- [55]Lukens LN, Doebley J: Epistatic and environmental interactions for quantitative trait loci involved in maize evolution. Genet Res 1999, 74:291-302.
- [56]Studer AJ, Doebley JF: Evidence for a natural allelic series at the maize domestication locus teosinte branched1. Genetics 2012, 191:951-958.
PDF