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Current Genomics

Editor-in-Chief

ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

General Research Article

Genome-wide Identification, Evolution and Expression Analysis of Basic Helix-loop-helix (bHLH) Gene Family in Barley (Hordeum vulgare L.)

Author(s): Qinglin Ke, Wenjing Tao, Tingting Li, Wenqiu Pan, Xiaoyun Chen, Xiaoyu Wu, Xiaojun Nie and Licao Cui*

Volume 21, Issue 8, 2020

Page: [624 - 644] Pages: 21

DOI: 10.2174/1389202921999201102165537

Price: $65

Abstract

Background: The basic helix-loop-helix (bHLH) transcription factor is one of the most important gene families in plants, playing a key role in diverse metabolic, physiological, and developmental processes. Although it has been well characterized in many plants, the significance of the bHLH family in barley is not well understood at present.

Methods: Through a genome-wide search against the updated barley reference genome, the genomic organization, evolution and expression of the bHLH family in barley were systematically analyzed.

Results: We identified 141 bHLHs in the barley genome (HvbHLHs) and further classified them into 24 subfamilies based on phylogenetic analysis. It was found that HvbHLHs in the same subfamily shared a similar conserved motif composition and exon-intron structures. Chromosome distribution and gene duplication analysis revealed that segmental duplication mainly contributed to the expansion of HvbHLHs and the duplicated genes were subjected to strong purifying selection. Furthermore, expression analysis revealed that HvbHLHs were widely expressed in different tissues and also involved in response to diverse abiotic stresses. The co-expression network was further analyzed to underpin the regulatory function of HvbHLHs. Finally, 25 genes were selected for qRT-PCR validation, the expression profiles of HvbHLHs showed diverse patterns, demonstrating their potential roles in relation to stress tolerance regulation.

Conclusion: This study reported the genome organization, evolutionary characteristics and expression profile of the bHLH family in barley, which not only provide the targets for further functional analysis, but also facilitate better understanding of the regulatory network bHLH genes involved in stress tolerance in barley.

Keywords: Barley, bHLH family, expression profile, qRT-PCR, transcription factor, helix-loop-helix.

Graphical Abstract

[1]
Ledent, V.; Vervoort, M. The basic helix-loop-helix protein family: comparative genomics and phylogenetic analysis. Genome Res., 2001, 11(5), 754-770.
[http://dx.doi.org/10.1101/gr.177001] [PMID: 11337472]
[2]
Carretero-Paulet, L.; Galstyan, A.; Roig-Villanova, I.; Martínez-García, J.F.; Bilbao-Castro, J.R.; Robertson, D.L. Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol., 2010, 153(3), 1398-1412.
[http://dx.doi.org/10.1104/pp.110.153593] [PMID: 20472752]
[3]
Feller, A.; Machemer, K.; Braun, E.L.; Grotewold, E. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J., 2011, 66(1), 94-116.
[http://dx.doi.org/10.1111/j.1365-313X.2010.04459.x] [PMID: 21443626]
[4]
Murre, C.; McCaw, P.S.; Baltimore, D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell, 1989, 56(5), 777-783.
[http://dx.doi.org/10.1016/0092-8674(89)90682-x] [PMID: 2493990]
[5]
Atchley, W.R.; Terhalle, W.; Dress, A. Positional dependence, cliques, and predictive motifs in the bHLH protein domain. J. Mol. Evol., 1999, 48(5), 501-516.
[http://dx.doi.org/10.1007/pl00006494] [PMID: 10198117]
[6]
Massari, M.E.; Murre, C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol., 2000, 20(2), 429-440.
[http://dx.doi.org/10.1128/mcb.20.2.429-440.2000] [PMID: 10611221]
[7]
Li, X.; Duan, X.; Jiang, H.; Sun, Y.; Tang, Y.; Yuan, Z.; Guo, J.; Liang, W.; Chen, L.; Yin, J. Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol., 2006, 141(4), 1167-1184.
[http://dx.doi.org/10.1104/pp.106.080580] [PMID: 16896230]
[8]
Niu, X.; Guan, Y.; Chen, S.; Li, H. Genome-wide analysis of basic helix-loop-helix (bHLH) transcription factors in Brachypodium distachyon. BMC Genomics, 2017, 18(1), 619.
[http://dx.doi.org/10.1186/s12864-017-4044-4] [PMID: 28810832]
[9]
Wei, K.; Chen, H. Comparative functional genomics analysis of bHLH gene family in rice, maize and wheat. BMC Plant Biol., 2018, 18(1), 309.
[http://dx.doi.org/10.1186/s12870-018-1529-5] [PMID: 30497403]
[10]
Zhang, T.; Lv, W.; Zhang, H.; Ma, L.; Li, P.; Ge, L.; Li, G. Genome-wide analysis of the basic Helix-Loop-Helix (bHLH) transcription factor family in maize. BMC Plant Biol., 2018, 18(1), 235.
[http://dx.doi.org/10.1186/s12870-018-1441-z] [PMID: 30326829]
[11]
Ke, Y.Z.; Wu, Y.W.; Zhou, H.J.; Chen, P.; Wang, M.M.; Liu, M.M.; Li, P.F.; Yang, J.; Li, J.N.; Du, H. Genome-wide survey of the bHLH super gene family in Brassica napus. BMC Plant Biol., 2020, 20(1), 115.
[http://dx.doi.org/10.1186/s12870-020-2315-8] [PMID: 32171243]
[12]
Hwang, Y.; Choi, H.S. Tracheophytes contain conserved orthologs of a basic helix-loop-helix transcription factor that modulate ROOT HAIR SPECIFIC genes. Plant Cell, 2017, 29(1), 39-53.
[http://dx.doi.org/10.1105/tpc.16.00732] [PMID: 28087829]
[13]
Zhu, E.; You, C.; Wang, S.; Cui, J.; Niu, B.; Wang, Y.; Qi, J.; Ma, H.; Chang, F. The DYT1-interacting proteins bHLH010, bHLH089 and bHLH091 are redundantly required for Arabidopsis anther development and transcriptome. Plant J., 2015, 83(6), 976-990.
[http://dx.doi.org/10.1111/tpj.12942] [PMID: 26216374]
[14]
Li, S.; Wang, X.; He, S.; Li, J.; Huang, Q.; Imaizumi, T.; Qu, L.; Qin, G.; Qu, L.J.; Gu, H. CFLAP1 and CFLAP2 are two bHLH transcription factors participating in synergistic regulation of AtCFL1-mediated cuticle development in arabidopsis. PLoS Genet., 2016, 12(1)e1005744
[http://dx.doi.org/10.1371/journal.pgen.1005744] [PMID: 26745719]
[15]
Luo, J.; Liu, H.; Zhou, T.; Gu, B.; Huang, X.; Shangguan, Y.; Zhu, J.; Li, Y.; Zhao, Y.; Wang, Y. An-1 encodes a basic helix-loop-helix protein that regulates awn development, grain size, and grain number in rice. Plant Cell, 2013, 25(9), 3360-3376.
[http://dx.doi.org/10.1105/tpc.113.113589] [PMID: 24076974]
[16]
Liu, Y.; Ji, X.; Nie, X.; Qu, M.; Zheng, L.; Tan, Z.; Zhao, H.; Huo, L.; Liu, S.; Zhang, B. Arabidopsis AtbHLH112 regulates the expression of genes involved in abiotic stress tolerance by binding to their E-box and GCG-box motifs. New Phytol., 2015, 207(3), 692-709.
[http://dx.doi.org/10.1111/nph.13387] [PMID: 25827016]
[17]
Seo, J.S.; Joo, J.; Kim, M.J.; Kim, Y.K.; Nahm, B.H.; Song, S.I.; Cheong, J.J.; Lee, J.S.; Kim, J.K.; Choi, Y.D. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J., 2011, 65(6), 907-921.
[http://dx.doi.org/10.1111/j.1365-313X.2010.04477.x] [PMID: 21332845]
[18]
Kiribuchi, K.; Sugimori, M.; Takeda, M.; Otani, T.; Okada, K.; Onodera, H.; Ugaki, M.; Tanaka, Y.; Tomiyama-Akimoto, C.; Yamaguchi, T. RERJ1, a jasmonic acid-responsive gene from rice, encodes a basic helix-loop-helix protein. Biochem. Biophys. Res. Commun., 2004, 325(3), 857-863.
[http://dx.doi.org/10.1016/j.bbrc.2004.10.126] [PMID: 15541369]
[19]
Lau, O.S.; Song, Z.; Zhou, Z.; Davies, K.A.; Chang, J.; Yang, X.; Wang, S.; Lucyshyn, D.; Tay, I.H.Z.; Wigge, P.A. Direct control of SPEECHLESS by PIF4 in the high-temperature response of stomatal development. Curr. Biol., 2018, 28(8), 1273-1280.e1273.
[http://dx.doi.org/10.1016/j.cub.2018.02.054] [PMID: 29628371]
[20]
Wang, Y.J.; Zhang, Z.G.; He, X.J.; Zhou, H.L.; Wen, Y.X.; Dai, J.X.; Zhang, J.S.; Chen, S.Y. A rice transcription factor OsbHLH1 is involved in cold stress response. Theor. Appl. Genet., 2003, 107(8), 1402-1409.
[http://dx.doi.org/10.1007/s00122-003-1378-x] [PMID: 12920519]
[21]
Martín, G.; Rovira, A.; Veciana, N.; Soy, J.; Toledo-Ortiz, G.; Gommers, C.M.M.; Boix, M.; Henriques, R.; Minguet, E.G.; Alabadí, D. Circadian waves of transcriptional repression shape PIF-regulated photoperiod-responsive growth in Arabidopsis. Curr. Biol., 2018, 28(2), 311-318.e315.
[http://dx.doi.org/10.1016/j.cub.2017.12.021] [PMID: 29337078]
[22]
Li, K.; Yu, R.; Fan, L.M.; Wei, N.; Chen, H. DELLA-mediated PIF degradation contributes to coordination of light and gibberellin signalling in Arabidopsis. Nat. Commun., 2016, 7, 11868.
[http://dx.doi.org/10.1038/ncomms11868] [PMID: 27282989]
[23]
Chandler, J.W.; Cole, M.; Flier, A.; Werr, W. BIM1, a bHLH protein involved in brassinosteroid signalling, controls Arabidopsis embryonic patterning via interaction with DORNROSCHEN and DORNROSCHEN-LIKE. Plant Mol. Biol., 2009, 69(1-2), 57-68.
[http://dx.doi.org/10.1007/s11103-008-9405-6] [PMID: 18830673]
[24]
Tian, H.; Guo, H.; Dai, X.; Cheng, Y.; Zheng, K.; Wang, X.; Wang, S. An ABA down-regulated bHLH transcription repressor gene, bHLH129 regulates root elongation and ABA response when overexpressed in Arabidopsis. Sci. Rep., 2015, 5, 17587.
[http://dx.doi.org/10.1038/srep17587] [PMID: 26625868]
[25]
Takahashi, Y.; Kinoshita, T.; Matsumoto, M.; Shimazaki, K. Inhibition of the Arabidopsis bHLH transcription factor by monomerization through abscisic acid-induced phosphorylation. Plant J., 2016, 87(6), 559-567.
[http://dx.doi.org/10.1111/tpj.13217] [PMID: 27227462]
[26]
Wang, H.; Li, Y.; Pan, J.; Lou, D.; Hu, Y.; Yu, D. The bHLH transcription factors MYC2, MYC3, and MYC4 are required for jasmonate-mediated inhibition of flowering in arabidopsis. Mol. Plant, 2017, 10(11), 1461-1464.
[http://dx.doi.org/10.1016/j.molp.2017.08.007] [PMID: 28827172]
[27]
Cui, Y.; Chen, C.L.; Cui, M.; Zhou, W.J.; Wu, H.L.; Ling, H.Q. Four IVa bHLH transcription factors are novel interactors of FIT and mediate JA inhibition of iron uptake in arabidopsis. Mol. Plant, 2018, 11(9), 1166-1183.
[http://dx.doi.org/10.1016/j.molp.2018.06.005] [PMID: 29960107]
[28]
Mascher, M.; Gundlach, H.; Himmelbach, A.; Beier, S.; Twardziok, S.O.; Wicker, T.; Radchuk, V.; Dockter, C.; Hedley, P.E.; Russell, J. A chromosome conformation capture ordered sequence of the barley genome. Nature, 2017, 544(7651), 427-433.
[http://dx.doi.org/10.1038/nature22043] [PMID: 28447635]
[29]
Chen, L.; Hu, W.; Tan, S.; Wang, M.; Ma, Z.; Zhou, S.; Deng, X.; Zhang, Y.; Huang, C.; Yang, G. Genome-wide identification and analysis of MAPK and MAPKK gene families in Brachypodium distachyon. PLoS One, 2012, 7(10)e46744
[http://dx.doi.org/10.1371/journal.pone.0046744] [PMID: 23082129]
[30]
Ostlund, G.; Schmitt, T.; Forslund, K.; Köstler, T.; Messina, D.N.; Roopra, S.; Frings, O.; Sonnhammer, E.L. InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res., 2010, 38(Database issue), D196-D203.
[http://dx.doi.org/10.1093/nar/gkp931] [PMID: 19892828]
[31]
Wang, Y.; Tang, H.; Debarry, J.D.; Tan, X.; Li, J.; Wang, X.; Lee, T.H.; Jin, H.; Marler, B.; Guo, H. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res., 2012, 40(7)e49
[http://dx.doi.org/10.1093/nar/gkr1293] [PMID: 22217600]
[32]
Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol., 2007, 24(8), 1586-1591.
[http://dx.doi.org/10.1093/molbev/msm088] [PMID: 17483113]
[33]
Pertea, M.; Kim, D.; Pertea, G.M.; Leek, J.T.; Salzberg, S.L. Transcript-level expression analysis of RNA-seq experiments with HISAT. StringTie and Ballgown., 2016, 11(9), 1650-1667.
[http://dx.doi.org/10.1038/nprot.2016.095] [PMID: 27560171]
[34]
Yue, W.; Nie, X.; Cui, L.; Zhi, Y.; Zhang, T.; Du, X.; Song, W. Genome-wide sequence and expressional analysis of autophagy Gene family in bread wheat (Triticum aestivum L.). J. Plant Physiol., 2018, 229, 7-21.
[http://dx.doi.org/10.1016/j.jplph.2018.06.012] [PMID: 30025220]
[35]
Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Method. Methods, 2001, 25(4), 402-408.
[http://dx.doi.org/10.1006/meth.2001.1262] [PMID: 11846609]
[36]
Atchley, W.R.; Fitch, W.M. A natural classification of the basic helix-loop-helix class of transcription factors. Proc. Natl. Acad. Sci. USA, 1997, 94(10), 5172-5176.
[http://dx.doi.org/10.1073/pnas.94.10.5172] [PMID: 9144210]
[37]
Ferré-D’Amaré, A.R.; Pognonec, P.; Roeder, R.G.; Burley, S.K. Structure and function of the b/HLH/Z domain of USF. EMBO J., 1994, 13(1), 180-189.
[PMID: 8306960]
[38]
Shimizu, T.; Toumoto, A.; Ihara, K.; Shimizu, M.; Kyogoku, Y.; Ogawa, N.; Oshima, Y.; Hakoshima, T. Crystal structure of PHO4 bHLH domain-DNA complex: flanking base recognition. EMBO J., 1997, 16(15), 4689-4697.
[http://dx.doi.org/10.1093/emboj/16.15.4689] [PMID: 9303313]
[39]
Xu, G.; Guo, C.; Shan, H.; Kong, H. Divergence of duplicate genes in exon-intron structure. Proc. Natl. Acad. Sci. USA, 2012, 109(4), 1187-1192.
[http://dx.doi.org/10.1073/pnas.1109047109] [PMID: 22232673]
[40]
Pyle, A.M. The tertiary structure of group II introns: implications for biological function and evolution. Crit. Rev. Biochem. Mol. Biol., 2010, 45(3), 215-232.
[http://dx.doi.org/10.3109/10409231003796523] [PMID: 20446804]
[41]
Toledo-Ortiz, G.; Huq, E.; Quail, P.H. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell, 2003, 15(8), 1749-1770.
[http://dx.doi.org/10.1105/tpc.013839] [PMID: 12897250]
[42]
Bartel, D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2), 281-297.
[http://dx.doi.org/10.1016/s0092-8674(04)00045-5] [PMID: 14744438]
[43]
Lynch, M.; Conery, J.S. The evolutionary fate and consequences of duplicate genes. Science, 2000, 290(5494), 1151-1155.
[http://dx.doi.org/10.1126/science.290.5494.1151] [PMID: 11073452]
[44]
Purugganan, M.D. Evolutionary insights into the nature of plant domestication. Curr. Biol., 2019, 29(14), R705-R714.
[http://dx.doi.org/10.1016/j.cub.2019.05.053] [PMID: 31336092]
[45]
Purugganan, M.D.; Fuller, D.Q. The nature of selection during plant domestication. Nature, 2009, 457(7231), 843-848.
[http://dx.doi.org/10.1038/nature07895]
[46]
Lai, X.; Yan, L.; Lu, Y.; Schnable, J.C. Largely unlinked gene sets targeted by selection for domestication syndrome phenotypes in maize and sorghum. Plant J., 2018, 93(5), 843-855.
[http://dx.doi.org/10.1111/tpj.13806] [PMID: 29265526]
[47]
Schlereth, A.; Möller, B.; Liu, W.; Kientz, M.; Flipse, J.; Rademacher, E.H.; Schmid, M.; Jürgens, G.; Weijers, D. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature, 2010, 464(7290), 913-916.
[http://dx.doi.org/10.1038/nature08836] [PMID: 20220754]
[48]
Zhang, L.Y.; Bai, M.Y.; Wu, J.; Zhu, J.Y.; Wang, H.; Zhang, Z.; Wang, W.; Sun, Y.; Zhao, J.; Sun, X. Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell, 2009, 21(12), 3767-3780.
[http://dx.doi.org/10.1105/tpc.109.070441] [PMID: 20009022]
[49]
Liu, Y.; Li, X.; Li, K.; Liu, H.; Lin, C. Multiple bHLH proteins form heterodimers to mediate CRY2-dependent regulation of flowering-time in Arabidopsis. PLoS Genet., 2013, 9(10)e1003861
[http://dx.doi.org/10.1371/journal.pgen.1003861] [PMID: 24130508]
[50]
Castelain, M.; Le Hir, R.; Bellini, C. The non-DNA-binding bHLH transcription factor PRE3/bHLH135/ATBS1/TMO7 is involved in the regulation of light signaling pathway in Arabidopsis. Physiol. Plant., 2012, 145(3), 450-460.
[http://dx.doi.org/10.1111/j.1399-3054.2012.01600.x] [PMID: 22339648]
[51]
Petridis, A.; Döll, S.; Nichelmann, L.; Bilger, W.; Mock, H.P. Arabidopsis thaliana G2-LIKE FLAVONOID REGULATOR and BRASSINOSTEROID ENHANCED EXPRESSION1 are low-temperature regulators of flavonoid accumulation. New Phytol., 2016, 211(3), 912-925.
[http://dx.doi.org/10.1111/nph.13986] [PMID: 27125220]
[52]
Kondou, Y.; Nakazawa, M.; Kawashima, M.; Ichikawa, T.; Yoshizumi, T.; Suzuki, K.; Ishikawa, A.; Koshi, T.; Matsui, R.; Muto, S. RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiol., 2008, 147(4), 1924-1935.
[http://dx.doi.org/10.1104/pp.108.118364] [PMID: 18567831]
[53]
Komatsu, M.; Maekawa, M.; Shimamoto, K.; Kyozuka, J. The LAX1 and FRIZZY PANICLE 2 genes determine the inflorescence architecture of rice by controlling rachis-branch and spikelet development. Dev. Biol., 2001, 231(2), 364-373.
[http://dx.doi.org/10.1006/dbio.2000.9988] [PMID: 11237465]
[54]
de Marcos, A.; Houbaert, A. A mutation in the bHLH domain of the SPCH transcription factor uncovers a BR-dependent mechanism for stomatal development. 2017, 174(2), 823-842.
[http://dx.doi.org/10.1104/pp.17.00615] [PMID: 28507175]
[55]
Nakamura, Y.; Kato, T.; Yamashino, T.; Murakami, M.; Mizuno, T. Characterization of a set of phytochrome-interacting factor-like bHLH proteins in Oryza sativa. Biosci. Biotechnol. Biochem., 2007, 71(5), 1183-1191.
[http://dx.doi.org/10.1271/bbb.60643] [PMID: 17485859]
[56]
Ahmad, A.; Niwa, Y.; Goto, S.; Ogawa, T.; Shimizu, M.; Suzuki, A.; Kobayashi, K.; Kobayashi, H. bHLH106 integrates functions of multiple genes through their g-box to confer salt tolerance on arabidopsis. PLoS One, 2015, 10(5)e0126872
[http://dx.doi.org/10.1371/journal.pone.0126872] [PMID: 25978450]
[57]
Zheng, K.; Wang, Y.; Zhang, N.; Jia, Q.; Wang, X.; Hou, C.; Chen, J.G.; Wang, S. Involvement of PACLOBUTRAZOL RESISTANCE6/KIDARI, an atypical bHLH transcription factor, in auxin responses in Arabidopsis. Front. Plant Sci., 2017, 8, 1813.
[http://dx.doi.org/10.3389/fpls.2017.01813] [PMID: 29114256]
[58]
Tanabe, N.; Noshi, M.; Mori, D.; Nozawa, K.; Tamoi, M.; Shigeoka, S. The basic helix-loop-helix transcription factor, bHLH11 functions in the iron-uptake system in Arabidopsis thaliana. J. Plant Res., 2019, 132(1), 93-105.
[http://dx.doi.org/10.1007/s10265-018-1068-z] [PMID: 30417276]
[59]
Moreno, J.E.; Moreno-Piovano, G.; Chan, R.L. The antagonistic basic helix-loop-helix partners BEE and IBH1 contribute to control plant tolerance to abiotic stress. Plant Sci., 2018, 271, 143-150.
[http://dx.doi.org/10.1016/j.plantsci.2018.03.024] [PMID: 29650152]
[60]
Colangelo, E.P.; Guerinot, M.L. The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell, 2004, 16(12), 3400-3412.
[http://dx.doi.org/10.1105/tpc.104.024315] [PMID: 15539473]
[61]
Masuda, H.; Aung, M.S.; Kobayashi, T.; Hamada, T.; Nishizawa, N.K. Enhancement of iron acquisition in rice by the mugineic acid synthase gene with ferric iron reductase gene and OsIRO2 confers tolerance in submerged and nonsubmerged calcareous soils. Front. Plant Sci., 2019, 10, 1179.
[http://dx.doi.org/10.3389/fpls.2019.01179] [PMID: 31681346]
[62]
Ogo, Y.; Itai, R.N.; Kobayashi, T.; Aung, M.S.; Nakanishi, H.; Nishizawa, N.K. OsIRO2 is responsible for iron utilization in rice and improves growth and yield in calcareous soil. Plant Mol. Biol., 2011, 75(6), 593-605.
[http://dx.doi.org/10.1007/s11103-011-9752-6] [PMID: 21331630]
[63]
Ogo, Y.; Itai, R.N.; Nakanishi, H.; Kobayashi, T.; Takahashi, M.; Mori, S.; Nishizawa, N.K. The rice bHLH protein OsIRO2 is an essential regulator of the genes involved in Fe uptake under Fe-deficient conditions. Plant J., 2007, 51(3), 366-377.
[http://dx.doi.org/10.1111/j.1365-313X.2007.03149.x] [PMID: 17559517]
[64]
ZhiMing. Y.; Bo, K.; XiaoWei, H.; ShaoLei, L.; YouHuang, B.; WoNa, D.; Ming, C.; Hyung-Taeg, C.; Ping, W. Root hair-specific expansins modulate root hair elongation in rice. Plant J., 2011, 66(5), 725-734.
[http://dx.doi.org/10.1111/j.1365-313X.2011.04533.x] [PMID: 21309868]
[65]
Gómez, M.D.; Fuster-Almunia, C.; Ocaña-Cuesta, J.; Alonso, J.M.; Pérez-Amador, M.A. RGL2 controls flower development, ovule number and fertility in Arabidopsis. Plant Science: Int. J. Exp. Plant Biol., 2019, 281, 82-92.
[http://dx.doi.org/10.1016/j.plantsci.2019.01.014] [PMID: 30824064]
[66]
Oh, E.; Yamaguchi, S.; Hu, J.; Yusuke, J.; Jung, B.; Paik, I.; Lee, H.S.; Sun, T.P.; Kamiya, Y.; Choi, G. PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell, 2007, 19(4), 1192-1208.
[http://dx.doi.org/10.1105/tpc.107.050153] [PMID: 17449805]

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