Abstract
Key message
TaRNAC1 is a constitutively and predominantly root-expressed NAC transcription factor. TaRNAC1 overexpression in wheat roots confers increased root length, biomass and drought tolerance and improved grain yield under water limitation.
Abstract
A large and deep root system is an important trait for yield sustainability of dryland cereal crops in drought-prone environments. This study investigated the role of a predominantly root-expressed NAC transcription factor from wheat (TaRNAC1) in the root growth. Expression analysis showed that TaRNAC1 was a constitutively expressed gene with high level expression in the roots and was not drought-upregulated. Overexpression of TaRNAC1 in wheat using a predominantly root-expressed promoter resulted in increased root length and biomass observed at the early growth stage and a marked increase in the maturity root biomass with dry root weight of > 70% higher than that of the wild type plants. Analysis of some root growth-related genes revealed that the expression level of GA3-ox2, which encodes GIBBERELLIN 3-OXIDASE catalysing the conversion of inactive gibberellin (GA) to active GA, was elevated in the roots of transgenic wheat. TaRNAC1 overexpressing transgenic wheat showed more dehydration tolerance under polyethylene glycol (PEG) treatment and produced more aboveground biomass and grain under water-limited conditions than the wild type plants. These data suggest that TaRNAC1 may play a role in root growth and be used as a molecular tool for potential enlargement of root system in wheat.
Similar content being viewed by others
Abbreviations
- GA:
-
Gibberellin
- GFP:
-
Green fluorescent protein
- PEG:
-
Polyethylene glycol
- RFP:
-
Red fluorescent protein
References
Chang H, Chen D, Kam J, Richardson T, Drenth J, Guo X, McIntyre CL, Chai S, Rae AL, Xue GP (2016) Abiotic stress upregulated TaZFP34 represses the expression of type-B response regulator and SHY2 genes and enhances root to shoot ratio in wheat. Plant Sci 252:88–102
Chen D, Richardson T, Chai S, McIntyre CL, Rae AL, Xue GP (2016) Drought-up-regualated TaNAC69-1 is a transcriptional repressor of TaSHY2 and TaIAA7, and enhances root length and biomass in wheat. Plant Cell Physiol 57:2076–2090
Fang Y, Liao K, Du H, Xu Y, Song H, Li X, Xiong L (2015) A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J Exp Bot 66:6803–6817
Ghanem ME, Hichri I, Smigocki AC, Albacete A, Fauconnier ML, Diatloff E, Martinez-Andujar C, Lutts S, Dodd IC, Pérez-Alfocea F (2011) Root-targeted biotechnology to mediate hormonal signalling and improve crop stress tolerance. Plant Cell Rep 30:807–823
Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, Zou HF, Lei G, Tian AG, Zhang WK, Ma B, Zhang JS, Chen SY (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68:302–313
He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Rev. ed. by by Arnon DI. College of Agriculture, University of California in Berkeley, Calif, pp 1–32
Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145
Huang Q, Wang Y, Li B, Chang J, Chen M, Li K, Yang G, He G (2015) TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis. BMC Plant Biol 15:268
Ishida Y, Tsunashima M, Hiei Y, Komari T (2015) Wheat (Triticum aestivum L.) transformation using immature embryos. Methods Mol Boil 1223:189–198
Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Choi YD, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197
Jeong JS, Kim YS, Redillas MCFR, Jang G, Jung H, Bang SW, Choi YD, Ha SH, Reuzeau C, Kim JK (2013) OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant Biotechnol J 11:101–114
Kooiker M, Drenth J, Glassop D, McIntyre CL, Xue GP (2013) TaMYB13-1, a R2R3 MYB transcription factor, regulates the fructan synthetic pathway and contributes to enhanced fructan accumulation in bread wheat. J Exp Bot 64:3681–3696
Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18:263–276
Li X-I, Yang X, Hu Y-X, Yu X-D, Li Q-L (2014) A novel NAC transcription factor from Suaeda liaotungensis K. enhanced transgenic Arabidopsisdrought, salt, and cold stress tolerance. Plant Cell Rep 33:767–778
Long SP, Ort DR (2010) More than taking the heat: crops and global change. Curr Opin Plant Biol 13:240–247
Lopes MS, Reynolds MP (2010) Partitioning of assimilates to deeper roots is associated with cooler canopies and increased yield under drought in wheat. Funct Plant Biol 37:147–156
Martin K, Kopperud K, Chakrabarty R, Banerjee R, Brooks R, Goodin MM (2009) Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant J 59:150–162
Maugarny-Calès A, Gonçalves B, Jouannic S, Melkonian M, Wong GKS, Laufs P (2016) Apparition of the NAC transcription factors predates the emergence of land plants. Mol Plant 9:1345–1348
Meister R, Rajani MS, Ruzicka D, Schachtman DP (2014) Challenges of modifying root traits in crops for agriculture. Trends Plant Sci 19:779–788
Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103
Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44
Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87
Pacifici E, Polverari L, Sabatini S (2015) Plant hormone cross-talk: the pivot of root growth. J Exp Bot 66:1113–1121
Podzimska-Sroka D, O’Shea C, Gregersen PL, Skriver K (2015) NAC transcription factors in senescence: from molecular structure to function in crops. Plants 4:412–448
Quach TN, Tran LSP, Valliyodan B, Nguyen HTM, Kumar R, Neelakandan AK, Guttikonda SK, Sharp RE, Nguyen HT (2014) Functional analysis of water stress-responsive soybean GmNAC003 and GmNAC004 transcription factors in lateral root development in Arabidopsis. PLoS One 9:e84886
Redillas MCFR, Jeong JS, Kim YS, Jung H, Bang SW, Choi YD, Ha SH, Reuzeau C, Kim JK (2012) The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnol J 10:792–805
Rogers ED, Benfey PN (2015) Regulation of plant root system architecture: implications for crop advancement. Curr Opi Biotechnol 32:93–98
Shaw LM, McIntyre CL, Gresshoff PM, Xue GP (2009) Members of the Dof transcription factor family in Triticum aestivum are associated with light-mediated gene regulation. Funct Integr Genomics 9:485–498
Song SY, Chen Y, Chen J, Dai XY, Zhang WH (2011) Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. Planta 234:331–345
Takasaki H, Maruyama k, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics 284:173–183
Tanimoto E (2012) Tall or short? Slender or thick? A plant strategy for regulating elongation growth of roots by low concentrations of gibberellin. Ann Bot 110:373–381
Thirumalaikumar VP, Devkar V, Mehterov N, Ali S, Ozgur R, Turkan I, Mueller-Roeber B, Balazadeh S (2017) NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato. Plant Biotechnol J. doi:10.1111/pbi.1277
Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45:1097–1102
Wasson AP, Richards RA, Chatrath R, Misra SC, Prasad SVS, Rebetzke GJ, Kirkegaard JA, Christopher J, Watt M (2012) Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. J Exp Bot 63:3485–3498
Xue GP, Loveridge CW (2004) HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. Plant J 37:326–339
Xue GP, McIntyre CL, Jenkins CLD, Glassop D, van Herwaarden AF, Shorter R (2008) Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiol 146:441–454
Xue GP, Way HM, Richardson T, Drenth J, Joyce PA, McIntyre CL (2011) Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol Plant 4:697–712
Xue GP, Drenth J, Glassop D, Kooiker M, McIntyre CL (2013) Dissecting the molecular basis of the contribution of source strength to high fructan accumulation in wheat. Plant Mol Biol 81:71–92
Xue GP, Rae AL, White R, Drenth J, Richardson T, McIntyre CL (2016) A strong root-specific expression system for stable transgene expression in bread wheat. Plant Cell Rep 35:469–481
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251
Yang X, Wang X, Ji L, Yi Z, Fu C, Ran J, Hu R, Zhou G (2015) Overexpression of a Miscanthus lutarioriparius NAC gene MlNAC5 confers enhanced drought and cold tolerance in Arabidopsis. Plant cell rep 34:943–958
Zhao X, Yang X, Pei S, He G, Wang X, Tang Q, Jia C, Lu Y, Hu R, Zhou (2016) The Miscanthus NAC transcription factor MlNAC9 enhances abiotic stress tolerance in transgenic. Arabidopsis Gene 586:158–169
Acknowledgements
This work is supported by CSIRO and the scholarship (D.C.) from China Scholarship Council (CSC). Authors are grateful to Terese Richardson, Smitha Louis and Dhara Bhatt for production of transgenic wheat, Janneke Drenth for her excellent technical assistance and Terry Grant for maintenance of plant growth facilities.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that there are no conflicts of interest.
Additional information
Communicated by Prakash Lakshmanan.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chen, D., Chai, S., McIntyre, C.L. et al. Overexpression of a predominantly root-expressed NAC transcription factor in wheat roots enhances root length, biomass and drought tolerance. Plant Cell Rep 37, 225–237 (2018). https://doi.org/10.1007/s00299-017-2224-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-017-2224-y