Overexpression of a predominantly root-expressed NAC transcription factor in wheat roots enhances root length, biomass and drought tolerance

Key messageTaRNAC1 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.AbstractA 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.

[1]  M. Melkonian,et al.  Apparition of the NAC Transcription Factors Predates the Emergence of Land Plants. , 2016, Molecular plant.

[2]  Jukon Kim,et al.  Root-Specific Expression of OsNAC10 Improves Drought Tolerance and Grain Yield in Rice under Field Drought Conditions1[W][OA] , 2010, Plant Physiology.

[3]  G. Xue,et al.  Drought-Up-Regulated TaNAC69-1 is a Transcriptional Repressor of TaSHY2 and TaIAA7, and Enhances Root Length and Biomass in Wheat. , 2016, Plant & cell physiology.

[4]  S. Chen,et al.  AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. , 2005, The Plant journal : for cell and molecular biology.

[5]  Donald R Ort,et al.  More than taking the heat: crops and global change. , 2010, Current opinion in plant biology.

[6]  C. O'Shea,et al.  NAC Transcription Factors in Senescence: From Molecular Structure to Function in Crops , 2015, Plants.

[7]  K. Shinozaki,et al.  The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice , 2010, Molecular Genetics and Genomics.

[8]  Guang-xiao Yang,et al.  TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis , 2015, BMC Plant Biology.

[9]  J. Drenth,et al.  TaMYB13-1, a R2R3 MYB transcription factor, regulates the fructan synthetic pathway and contributes to enhanced fructan accumulation in bread wheat , 2013, Journal of experimental botany.

[10]  T. Komari,et al.  Wheat (Triticum aestivum L.) transformation using immature embryos. , 2015, Methods in molecular biology.

[11]  R. Richards,et al.  Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. , 2012, Journal of experimental botany.

[12]  J. Drenth,et al.  Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. , 2011, Molecular plant.

[13]  M. Reynolds,et al.  Partitioning of assimilates to deeper roots is associated with cooler canopies and increased yield under drought in wheat , 2010 .

[14]  R. E. Sharp,et al.  Functional Analysis of Water Stress-Responsive Soybean GmNAC003 and GmNAC004 Transcription Factors in Lateral Root Development in Arabidopsis , 2014, PloS one.

[15]  J. Drenth,et al.  Abiotic stress upregulated TaZFP34 represses the expression of type-B response regulator and SHY2 genes and enhances root to shoot ratio in wheat. , 2016, Plant science : an international journal of experimental plant biology.

[16]  G. Xue,et al.  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. , 2004, The Plant journal : for cell and molecular biology.

[17]  L. Xiong,et al.  A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice , 2015, Journal of experimental botany.

[18]  Philip N Benfey,et al.  Regulation of plant root system architecture: implications for crop advancement. , 2015, Current opinion in biotechnology.

[19]  Biao Ma,et al.  Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. , 2011, The Plant journal : for cell and molecular biology.

[20]  Addie Nina Olsen,et al.  NAC transcription factors: structurally distinct, functionally diverse. , 2005, Trends in plant science.

[21]  D. R. Hoagland,et al.  The Water-Culture Method for Growing Plants Without Soil , 2018 .

[22]  Shoshi Kikuchi,et al.  Genome-wide analysis of NAC transcription factor family in rice. , 2010, Gene.

[23]  J. Drenth,et al.  Dissecting the molecular basis of the contribution of source strength to high fructan accumulation in wheat , 2012, Plant Molecular Biology.

[24]  K. Shinozaki,et al.  NAC transcription factors in plant abiotic stress responses. , 2012, Biochimica et biophysica acta.

[25]  Zili Yi,et al.  Overexpression of a Miscanthus lutarioriparius NAC gene MlNAC5 confers enhanced drought and cold tolerance in Arabidopsis , 2015, Plant Cell Reports.

[26]  D. Schachtman,et al.  Challenges of modifying root traits in crops for agriculture. , 2014, Trends in plant science.

[27]  Jie Chen,et al.  Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress , 2011, Planta.

[28]  Jukon Kim,et al.  OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. , 2013, Plant biotechnology journal.

[29]  E. Tanimoto.  Tall or short? Slender or thick? A plant strategy for regulating elongation growth of roots by low concentrations of gibberellin. , 2012, Annals of botany.

[30]  M. Yano,et al.  Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions , 2013, Nature Genetics.

[31]  S. Sabatini,et al.  Plant hormone cross-talk: the pivot of root growth. , 2015, Journal of experimental botany.

[32]  Kazuo Shinozaki,et al.  Genome-Wide Survey and Expression Analysis of the Plant-Specific NAC Transcription Factor Family in Soybean During Development and Dehydration Stress , 2011, DNA research : an international journal for rapid publication of reports on genes and genomes.

[33]  Qian Gao,et al.  Comprehensive Analysis of NAC Domain Transcription Factor Gene Family in Populus trichocarpa , 2010, BMC Plant Biology.

[34]  Xiaoyu Wang,et al.  The Miscanthus NAC transcription factor MlNAC9 enhances abiotic stress tolerance in transgenic Arabidopsis. , 2016, Gene.

[35]  M. Goodin,et al.  Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. , 2009, The Plant journal : for cell and molecular biology.

[36]  J. Drenth,et al.  A strong root-specific expression system for stable transgene expression in bread wheat , 2015, Plant Cell Reports.

[37]  B. Mueller‐Roeber,et al.  NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato , 2017, Plant biotechnology journal.

[38]  Shinjiro Yamaguchi,et al.  Gibberellin metabolism and its regulation. , 2008, Annual review of plant biology.

[39]  Xiao-dong Yu,et al.  A novel NAC transcription factor from Suaeda liaotungensis K. enhanced transgenic Arabidopsis drought, salt, and cold stress tolerance , 2014, Plant Cell Reports.

[40]  S. Lutts,et al.  Root-targeted biotechnology to mediate hormonal signalling and improve crop stress tolerance , 2011, Plant Cell Reports.

[41]  Jukon Kim,et al.  The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. , 2012, Plant biotechnology journal.

[42]  G. Xue,et al.  Molecular Dissection of Variation in Carbohydrate Metabolism Related to Water-Soluble Carbohydrate Accumulation in Stems of Wheat1[W] , 2007, Plant Physiology.

[43]  G. Xue,et al.  Members of the Dof transcription factor family in Triticum aestivum are associated with light-mediated gene regulation , 2009, Functional & Integrative Genomics.