Advertisement

Planta

, Volume 246, Issue 5, pp 1019–1028 | Cite as

Altered expression of the TaRSL2 gene contributed to variation in root hair length during allopolyploid wheat evolution

  • Haiming Han
  • Huifang Wang
  • Yao Han
  • Zhaorong Hu
  • Mingming Xin
  • Huiru Peng
  • Yingyin Yao
  • Qixin Sun
  • Zhongfu NiEmail author
Original Article

Abstract

Main conclusion

Altered expression of the TaRSL2 gene was positively correlated with variation in root hair length during allopolyploid wheat evolution, and overexpression of TaRSL2 in Arabidopsis increases root hair length.

Root hairs aid nutrient and water uptake and anchor the plant in the soil. Allopolyploid wheats display significant growth vigor in terms of root hair length compared to their diploid progenitors, but little is known about the molecular basis of variation in root hair length during wheat allopolyploidization. Here, we isolated three orthologs of the Arabidopsis root hair gene ROOT HAIR DEFECTIVE SIX-LIKE 2 (AtRSL2) in allohexaploid wheat, designated TaRSL2-4A, TaRSL2-4B and TaRSL2-4D. The deduced polypeptides of these three TaRSL2 homoeologous genes shared high similarity, and a conserved basic helix-loop-helix (bHLH) domain was present in their C-terminal regions. Notably, the expression of TaRSL2 was positively correlated with root hair length of wheat accessions with different ploidy levels. Moreover, ectopic overexpression of TaRSL2-4D in Arabidopsis could increase root hair length. We found that the transcript levels of TaRSL2 homoeologous genes dynamically changed during allopolyploid wheat evolution, implicating the complexity of the underlying molecular mechanism. Collectively, we propose that altered expression of the TaRSL2 gene contributed to variation in root hair length in allopolyploid wheats.

Keywords

Gene expression Polyploidization ROOT HAIR DEFECTIVE SIX-LIKETriticum aestivum 

Abbreviations

bHLH

Basic helix-loop-helix

RSL

ROOT HAIR DEFECTIVE SIX-LIKE

Notes

Acknowledgements

This research was supported by grants from the Major Program of the National Natural Science Foundation of China (31290212) and the National Key Research and Development Program of China (Grant No. 2016YFD0100801).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

425_2017_2735_MOESM1_ESM.pdf (2.5 mb)
Supplementary material 1 (PDF 2539 kb)

References

  1. Akhunova AR, Matniyazov RT, Liang HQ, Akhunov ED (2010) Homoeolog-specific transcriptional bias in allopolyploid wheat. BMC Genom 11:505. doi: 10.1186/1471-2164-11-505 CrossRefGoogle Scholar
  2. Balao F, Herrera J, Talavera S (2011) Phenotypic consequences of polyploidy and genome size at the microevolutionary scale: a multivariate morphological approach. N Phytol 192:256–265CrossRefGoogle Scholar
  3. Brown LK, George TS, Thompson JA, Wright G, Lyon J, Dupuy L, Hubbard SF, White PJ (2012) What are the implications of variation in root hair length on tolerance to phosphorus deficiency in combination with water stress in barley (Hordeum vulgare)? Ann Bot 110:319–328CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bruex A, Kainkaryam RM, Wieckowski Y, Kang YH, Bernhardt C, Xia Y, Zheng XH, Wang JY, Lee MM, Benfey P, Woolf PJ, Schiefelbein J (2012) A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet 8(1):e1002446. doi: 10.1371/journal.pgen.1002446 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406CrossRefPubMedPubMedCentralGoogle Scholar
  6. Clarke JD (2009) Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harbor Protocols 2009, pdb. prot5177Google Scholar
  7. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  8. Datta S, Kim CM, Pernas M, Pires ND, Proust H, Tam T, Vijayakumar P, Dolan L (2011) Root hairs: development, growth and evolution at the plant-soil interface. Plant Soil 346:1–14CrossRefGoogle Scholar
  9. Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316:1862–1866CrossRefPubMedPubMedCentralGoogle Scholar
  10. Feldman M, Levy AA (2005) Allopolyploidy-a shaping force in the evolution of wheat genomes. Cytogenet Genome Res 109:250–258CrossRefPubMedGoogle Scholar
  11. Feldman M, Lupton FGH, Miller TE (1995) Wheats. In: Smartt J, Simmonds NW (eds) Evolution of crop plants, 2nd edn. Longman Scientific, London, pp 184–192Google Scholar
  12. Feldman M, Levy AA, Fahima T, Korol A (2012) Genomic asymmetry in allopolyploid plants: wheat as a model. J Exp Bot 63:5045–5059CrossRefPubMedGoogle Scholar
  13. Franciosini A, Rymen B, Shibata M, Favero DS, Sugimoto K (2017) Molecular networks orchestrating plant cell growth. Curr Opin Plant Biol 35:98–104CrossRefPubMedGoogle Scholar
  14. Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60CrossRefPubMedGoogle Scholar
  15. Haling RE, Brown LK, Bengough AG, Young IM, Hallett PD, White PJ, George TS (2013) Root hairs improve root penetration, root-soil contact, and phosphorus acquisition in soils of different strength. J Exp Bot 64:3711–3721CrossRefPubMedGoogle Scholar
  16. Han Y, Xin M, Huang K, Xu Y, Liu Z, Hu Z, Yao Y, Peng H, Ni Z, Sun Q (2016) Altered expression of TaRSL4 gene by genome interplay shapes root hair length in allopolyploid wheat. N Phytol 209:721–732CrossRefGoogle Scholar
  17. He X, Zeng J, Cao F, Ahmed IM, Zhang G, Vincze E, Wu F (2015) HvEXPB7, a novel beta-expansin gene revealed by the root hair transcriptome of Tibetan wild barley, improves root hair growth under drought stress. J Exp Bot 66:7405–7419CrossRefPubMedPubMedCentralGoogle Scholar
  18. Horn R, Wingen LU, Snape JW, Dolan L (2016) Mapping of quantitative trait loci for root hair length in wheat identifies loci that co-locate with loci for yield components. J Exp Bot 67:4535–4543CrossRefPubMedPubMedCentralGoogle Scholar
  19. Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P (2002) Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc Natl Acad Sci USA 99:8133–8138CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hwang Y, Choi HS, Cho HM, Cho HT (2017) Tracheophytes contain conserved orthologs of a basic helix-loop-helix transcription factor to modulate ROOT HAIR SPECIFIC genes. Plant Cell 29:39–53CrossRefPubMedPubMedCentralGoogle Scholar
  21. Jackson S, Chen ZJ (2010) Genomic and expression plasticity of polyploidy. Curr Opin Plant Biol 13:153–159CrossRefPubMedGoogle Scholar
  22. Kim CM, Dolan L (2016) ROOT HAIR DEFECTIVE SIX-LIKE Class I genes promote root hair development in the grass Brachypodium distachyon. PLoS Genet 12:e1006211. doi: 10.1371/journal.pgen.1006211 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kim DW, Lee SH, Choi SB, Won SK, Heo YK, Cho M, Park YI, Cho HT (2006) Functional conservation of a root hair cell-specific cis-element in angiosperms with different root hair distribution patterns. Plant Cell 18:2958–2970CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kim CM, Han CD, Dolan L (2017) RSL class I genes positively regulate root hair development in Oryza sativa. N Phytol 213:314–323CrossRefGoogle Scholar
  25. Kwasniewski M, Nowakowska U, Szumera J, Chwialkowska K, Szarejko I (2013) iRootHair: a comprehensive root hair genomics database. Plant Physiol 161:28–35CrossRefPubMedGoogle Scholar
  26. Li A, Liu D, Wu J, Zhao X, Hao M, Geng S, Yan J, Jiang X, Zhang L, Wu J, Yin L, Zhang R, Wu L, Zheng Y, Mao L (2014) mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant Cell 26:1878–1900CrossRefPubMedPubMedCentralGoogle Scholar
  27. Liu B, Xu CM, Zhao N, Qi B, Kimatu JN, Pang JS, Han FP (2009) Rapid genomic changes in polyploid wheat and related species: implications for genome evolution and genetic improvement. J Genet Genom 36:519–528CrossRefGoogle Scholar
  28. Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 24:459–467CrossRefGoogle Scholar
  29. Madlung A (2013) Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110:99–104CrossRefPubMedGoogle Scholar
  30. Marzec M, Melzer M, Szarejko I (2015) Root hair development in the grasses: what we already know and what we still need to know. Plant Physiol 168:407–414CrossRefPubMedPubMedCentralGoogle Scholar
  31. Meister R, Rajani MS, Ruzicka D, Schachtman DP (2014) Challenges of modifying root traits in crops for agriculture. Trends Plant Sci 19:779–788CrossRefPubMedGoogle Scholar
  32. Nomura T, Ishihara A, Yanagita RC, Endo TR, Iwamura H (2005) Three genomes differentially contribute to the biosynthesis of benzoxazinones in hexaploid wheat. Proc Natl Acad Sci USA 102:16490–16495CrossRefPubMedPubMedCentralGoogle Scholar
  33. Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ, Lee HS, Comai L, Madlung A, Doerge RW, Colot V, Martienssen RA (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141–147CrossRefPubMedGoogle Scholar
  34. Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–462CrossRefPubMedGoogle Scholar
  35. Peterson RL (1992) Adaptations of root structure in relation to biotic and abiotic factors. Can J Bot 70:661–675CrossRefGoogle Scholar
  36. Peterson RL, Farquhar ML (1996) Root hairs: specialized tubular cells extending root surfaces. Bot Rev 62:1–40CrossRefGoogle Scholar
  37. Shitsukawa N, Tahira C, Kassai K, Hirabayashi C, Shimizu T, Takumi S, Mochida K, Kawaura K, Ogihara Y, Murai K (2007) Genetic and epigenetic alteration among three homoeologous genes of a class E MADS box gene in hexaploid wheat. Plant Cell 19:1723–1737CrossRefPubMedPubMedCentralGoogle Scholar
  38. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  39. Willcox G (1998) Archaeobotanical evidence for the beginnings of agriculture in Southwest Asia. In: Damania AB, Valkoun J, Willcox G, Qualset CO (eds) The origins of agriculture and crop domestication. ICARDA, Aleppo, pp 25–38Google Scholar
  40. Yang CW, Zhao L, Zhang HK, Yang ZZ, Wang H, Wen SS, Zhang CY, Rustgi S, von Wettstein D, Liu B (2014) Evolution of physiological responses to salt stress in hexaploid wheat. Proc Natl Acad Sci USA 111:11882–11887CrossRefPubMedPubMedCentralGoogle Scholar
  41. Yi K, Menand B, Bell E, Dolan L (2010) A basic helix-loop-helix transcription factor controls cell growth and size in root hairs. Nat Genet 42:264–267CrossRefPubMedGoogle Scholar
  42. Zhang Z, Belcram H, Gornicki P, Charles M, Just J, Huneau C, Magdelenat G, Couloux A, Samain S, Gill BS, Rasmussen JB, Barbe V, Faris JD, Chalhoub B (2011) Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat. Proc Natl Acad Sci USA 108:18737–18742CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Haiming Han
    • 1
  • Huifang Wang
    • 1
  • Yao Han
    • 1
  • Zhaorong Hu
    • 1
  • Mingming Xin
    • 1
  • Huiru Peng
    • 1
  • Yingyin Yao
    • 1
  • Qixin Sun
    • 1
  • Zhongfu Ni
    • 1
    Email author
  1. 1.State Key Laboratory for Agrobiotechnology, Key Laboratory of Crop Heterosis and Utilization (MOE), Beijing Key Laboratory of Crop Genetic ImprovementChina Agricultural UniversityBeijingChina

Personalised recommendations