Abstract
The basic helix-loop-helix (bHLH) transcription factor family is the second largest in plants. bHLH transcription factor is not only universally involved in plant growth and metabolism, including photomorphogenesis, light signal transduction, and secondary metabolism, but also plays an important role in plant response to stress. However, the function of bHLH TFs in Pseudoroegneria species has not been studied yet. Pseudoroegneria (Nevski) Á. Löve is a perennial genus of the Triticeae. Pseudoroegneria species are mostly distributed in arid/semi-arid areas and they show good drought tolerance. In this study, we identified 152 PlbHLH TFs in Pseudoroegneria libanotica, which could be classified into 15 groups. Collinearity analysis indicates that 122 PlbHLH genes share homology with wbHLH genes in wheat, and it has lower homology with AtbHLH genes in Arabidopsis. Based on transcriptome profiling under an experiment with three PEG concentrations (0%, 10%, and 20%), 10 up-regulated genes and 11 down-regulated PlbHLH genes were screened. Among them, PlbHLH6, PlbHLH55 and PlbHLH64 as candidate genes may be the key genes related to drought tolerance response at germination, and they have been demonstrated to respond to drought, salt, oxidative, heat, and heavy metal stress in yeast. This study lays the foundation for an in-depth study of the biological roles of PlbHLHs in Pse. libanotica, and discovered new drought-tolerance candidate genes to enhance the genetic background of Triticeae crops.
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Data availability
All data are available in the manuscript, the supplementary materials, or at publicly accessible repositories. These data in the public repositories include germination RNA-seq data of Pse. libanotica in NCBI under BioProjectID PRJNA1018656.
References
An R, Liu XY, Wang R et al (2014) The over-expression of two transcription factors, ABS5/bHLH30 and ABS7/MYB101, leads to upwardly curly leaves. PLoS ONE 9:e107637. https://doi.org/10.1371/journal.pone.0107637
Bailey PC, Martin C, Toledo-Ortiz G et al (2003) Update on the basic helix-loop-helix transcription factor gene family in Arabidopsis thaliana. Plant Cell 15(11):2497–2502. https://doi.org/10.1105/tpc.151140
BassiriRad H, Caldwell MM (1992) Temporal changes in root growth and 15N uptake and water relations of two tussock grass species recovering from water stress. Physiol Plantarum 86:525–531. https://doi.org/10.1111/j.1399-3054.1992.tb02165.x
Busso CA, Richards JH (1995) Drought and clipping effects on tiller demography andgrowth of two tussock grasses in Utah. J Arid Environ 29:239–251. https://doi.org/10.1016/S0140-1963(05)80093-X
Busso CA, Richards JH, Chatterton NJ (1990) Nonstructural carbohydrates and spring regrowth of two cool-season grasses: interaction of drought and clipping. Rangeland Ecol Manag 43:336–343. https://doi.org/10.2307/3898928
Chen L, Wang WS, Wang T et al (2019) Methyl salicylate glucosylation regulates plant defense signaling and systemic acquired resistance. Plant Physiol 180(4):2167–2181. https://doi.org/10.1104/pp.19.00091
Chen C, Chen H, Zhang Y et al (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Cowan MF, Blomstedt CK, Norton SL et al (2020) Crop wild relatives as a genetic resource for generating low-cyanide, drought-tolerant Sorghum. Environ Exp Bot 169:103884. https://doi.org/10.1016/j.envexpbot.2019.103884
Ding CB, Zhou YH (2004) Advances in research on Pseudoroegneria in the Tribe Triticeae. J Agri Univ Sichuan 22:269–273. https://doi.org/10.1300/J064v24n01_09
Feller A, Machemer K, Braun EL et al (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66:94–116. https://doi.org/10.1111/j.1365-313X.2010.04459.x
Fraser LH, Greenall A, Carlyle C et al (2009) Adaptive phenotypic plasticity of Pseudoroegneria spicata: response of stomatal density, leaf area and biomass to changes in water supply and increased temperature. Ann Bot 103:769–775. https://doi.org/10.1093/aob/mcn252
Gong BY, Zhu W, Li S et al (2019) Molecular cytogenetic characterization of wheat-Elymus repens chromosomal translocation lines with resistance to Fusarium head blight and stripe rust. BMC Plant Biol 19:1–11. https://doi.org/10.1186/s12870-019-2208-x
Guo XJ, Wang JR (2017) Global identification, structural analysis and expression characterization of bHLH transcription factors in wheat. BMC Plant Biol 17(1):1–12. https://doi.org/10.1186/s12870-017-1038-y
Guo J, Sun B, He H et al (2021) Current understanding of bHLH transcription factors in plant abiotic stress tolerance. Int J Mol Sci 22:4921. https://doi.org/10.3390/ijms22094921
Hernandez JM, Feller A, Morohashi K et al (2007) The basic helix loop helix domain of maize R links transcriptional regulation and histone modifications by recruitment of an EMSY-related factor. Proc Natl Acad Sci USA 104(43):17222–17227. https://doi.org/10.1073/pnas.0705629104
Huibers RP, De Jong M, Dekter RW et al (2009) Disease-specific expression of host genes during downy mildew infection of Arabidopsis. Mol Plant Microbe in 22(9):1104–1115. https://doi.org/10.1094/MPMI-22-9-1104
Kashyap A, Garg P, Tanwar K et al (2022) Strategies for utilization of crop wild relatives in plant breeding programs. Theor Appl Genet 135:4151–4167. https://doi.org/10.1007/s00122-022-04220-x
Kurt F, Filiz E, Kurt B (2019) A key gene bHLH115 in iron homeostasis: comprehensive bioinformatics analyses in Arabidopsis, tomato, rice, and maize. Biometals 32:641–656. https://doi.org/10.1007/s10534-019-00199-z
Larson L, Kiemnec G (2003) Seedling growth and interference of diffuse knapweed (Centaurea diffusa) and Bluebunch Wheatgrass (Pseudoroegneria spicata). Weed Technol 17:79–83. https://doi.org/10.1614/0890-037X(2003)017[0079:SGAIOD]2.0.CO;2
Ledent V, Vervoort M (2001) The basic helix-loop-helix protein family: comparative genomics and phylogenetic analysis. Genome Res 11(5):754–770. https://doi.org/10.1101/gr.177001
Lescot M, Déhais P, Thijs G et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327. https://doi.org/10.1093/nar/30.1.325
Li XX, Duan XP, Jiang HX et al (2006) Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 141(4):1167–1184. https://doi.org/10.1104/pp.106.080580
Li JL, Wang T, Han J et al (2020) Genome-wide identification and characterization of cucumber bHLH family genes and the functional characterization of CsbHLH041 in NaCl and ABA tolerance in Arabidopsis and cucumber. BMC Plant Biol 20:1–20. https://doi.org/10.1186/s12870-020-02440-1
Li M, Sun L, Gu H et al (2021) Genome-wide characterization and analysis of bHLH transcription factors related to anthocyanin biosynthesis in spine grapes (Vitis davidii). Sci Rep 11:6863. https://doi.org/10.1038/s41598-021-85754-w
Liang G (2022) Iron uptake, signaling, and sensing in plants. Plant Commun. https://doi.org/10.1016/j.xplc.2022.100349
Liu JH, Peng T, Dai W (2014) Critical cis-acting elements and interacting transcription factors: key players associated with abiotic stress responses in plants. Plant Mol Biol Rep 32:303–317. https://doi.org/10.1007/s11105-013-0667-z
Mao K, Dong QL, Li C et al (2017) Genome wide identification and characterization of apple bHLH transcription factors and expression analysis in response to drought and salt stress. Front Plant Sci 8:480. https://doi.org/10.3389/fpls.2017.00480
Misra BB, Acharya BR, Granot D et al (2015) The guard cell metabolome: functions in stomatal movement and global food security. Front Plant Sci 6:334. https://doi.org/10.3389/fpls.2015.00334
Peng F, Wang C, Zhu J et al (2018) Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants. Planta 247:1395–1406. https://doi.org/10.1007/s00425-018-2872-3
Seo JS, Joo J, Kim MJ et al (2011) OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 65(6):907–921. https://doi.org/10.1111/j.1365-313X.2010.04477.x
Song MY, Wang HM, Wang Z et al (2021) Genome-wide characterization and analysis of bHLH transcription factors related to anthocyanin biosynthesis in Fig (Ficus carica L.). Front Plant Sci 12:730692. https://doi.org/10.3389/fpls.2021.730692
Szklarczyk D, Gable AL, Lyon D et al (2019) STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47(D1):D607-d613. https://doi.org/10.1093/nar/gky1131
Wang PF, Wang HL, Wang YM et al (2018) Analysis of bHLH genes from foxtail millet (Setaria italica) and their potential relevance to drought stress. PLoS ONE 13(11):e0207344. https://doi.org/10.1371/journal.pone.0207344
Wang F, Itai RN, Nozoye T et al (2020) The bHLH protein OsIRO3 is critical for plant survival and iron (Fe) homeostasis in rice (Oryza sativa L.) under Fe-deficient conditions. Soil Sci Plant Nutr 66(4):579–592. https://doi.org/10.1080/00380768.2020.1783966
Xu W, Zhang N, Jiao Y et al (2014) The grapevine basic helix-loop-helix (bHLH) transcription factor positively modulates CBF-pathway and confers tolerance to cold-stress in Arabidopsis. Mol Biol Rep 41:5329–5342. https://doi.org/10.1007/s11033-014-3404-2
Yang T, Yao S, Hao L et al (2016) Wheat bHLH-type transcription factor gene TabHLH1 is crucial in mediating osmotic stresses tolerance through modulating largely the ABA-associated pathway. Plant Cell Rep 35:2309–2323. https://doi.org/10.1007/s00299-016-2036-5
Yang GT, Boshoff WHP, Li HW et al (2021) Chromosomal composition analysis and molecular marker development for the novel Ug99-resistant wheat–Thinopyrum ponticum translocation line WTT34. Theor Appl Genet 134:1587–1599. https://doi.org/10.1007/s00122-021-03796-0
Yen C, Yang JL (2011) Triticeae biosystematics, vol 4. Chinese Agricultural Press, Beijing
Zhang T, Lv W, Zhang H et al (2018) Genome-wide analysis of the basic Helix-Loop-Helix (bHLH) transcription factor family in maize. BMC Plant Biol 18:235. https://doi.org/10.1186/s12870-018-1441-z
Zhang K, Sun Y, Li M et al (2021) CrUGT87A1, a UDP-sugar glycosyltransferases (UGTs) gene from Carex rigescens, increases salt tolerance by accumulating flavonoids for antioxidation in Arabidopsis thaliana. Plant Physiol Bioch 159:28–36. https://doi.org/10.1016/j.plaphy.2020.12.006
Zhao Q, Fan ZH, Qiu LN et al (2020) MdbHLH130, an apple bHLH transcription factor, confers water stress resistance by regulating stomatal closure and ROS homeostasis in transgenic tobacco. Front Plant Sci 11:543696. https://doi.org/10.3389/fpls.2020.543696
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This work was financially supported by the National Natural Science Foundation of China (32270388, 32200180), and the Science and Technology Bureau of Sichuan Province (2023NSFSC1995).
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XZ and HZ were involved in the final development of the project and manuscript preparation. XZ, XW, XY, QH performed the experiments and analyzed the data. XZ wrote the manuscript draft. DW, YW, HK, LS, XF, YZ participate in the completion of the work.
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Zhai, X., Wang, X., Yang, X. et al. Genome-wide identification of bHLH transcription factors and expression analysis under drought stress in Pseudoroegneria libanotica at germination. Physiol Mol Biol Plants 30, 467–481 (2024). https://doi.org/10.1007/s12298-024-01433-w
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DOI: https://doi.org/10.1007/s12298-024-01433-w