Expression patterns; Family genes; Gossypium arboreum; Cotton Fiber; Plant Science
Abstract :
[en] MAIN CONCLUSION: GL2-interacting-repressor (GIR) family members may contribute to fiber/fuzz formation via a newly discovered unique pathway in Gossypium arboreum. There are similarities between cotton fiber development and the formation of trichomes and root hairs. The GL2-interacting-repressors (GIRs) are crucial regulators of root hair and trichome formation. The GaFzl gene, annotated as GaGIR1, is negatively associated with trichome development and fuzz initiation. However, there is relatively little available information regarding the other GIR genes in cotton, especially regarding their effects on cotton fiber development. In this study, 21 GIR family genes were identified in the diploid cotton species Gossypium arboreum; these genes were divided into three groups. The GIR genes were characterized in terms of their phylogenetic relationships, structures, chromosomal distribution and evolutionary dynamics. These GIR genes were revealed to be unequally distributed on 12 chromosomes in the diploid cotton genome, with no GIR gene detected on Ga06. The cis-acting elements in the promoter regions were predicted to be responsive to light, phytohormones, defense activities and stress. The transcriptomic data and qRT-PCR results revealed that most GIR genes were not differentially expressed between the wild-type control and the fuzzless mutant line. Moreover, 14 of 21 family genes were expressed at high levels, indicating these genes may play important roles during fiber development and fuzz formation. Furthermore, Ga01G0231 was predominantly expressed in root samples, suggestive of a role in root hair formation rather than in fuzz initiation and development. The results of this study have enhanced our understanding of the GIR genes and their potential utility for improving cotton fiber through breeding.
Disciplines :
Agriculture & agronomy
Author, co-author :
Feng, Xiaoxu ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, Henan, China
Cheng, Hailiang; State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, Henan, China
Zuo, Dongyun; State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, Henan, China
Zhang, Youping; State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, Henan, China
Wang, Qiaolian; State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, Henan, China
Lv, Limin; State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, Henan, China
Li, Shuyan; State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, Henan, China
Yu, John Z; Southern Plains Agricultural Research Center, USDA-ARS, Crop Germplasm Research Unit, 2881 F&B Road, College Station, Texas, 77845, USA. john.yu@usda.gov
Song, Guoli ; State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, Henan, China. songguoli@caas.cn
Language :
English
Title :
Genome-wide identification and expression analysis of GL2-interacting-repressor (GIR) genes during cotton fiber and fuzz development.
Publication date :
2022
Journal title :
Planta
ISSN :
0032-0935
eISSN :
1432-2048
Publisher :
Springer Science and Business Media Deutschland GmbH, Germany
NSCF - National Natural Science Foundation of China USDA - United States Department of Agriculture
Funding text :
This work was funded by grants from the National Natural Science Foundation of China (No. 31621005), the National Natural Science Foundation of China (No. 31901581), the National Key R & D Plan of China (No. 2018YFD0100402) and the United States Department of Agriculture—Agricultural Research Service (USDA-ARS Project No. 3091-21000044-00D). The funders had no role in the experimental design, data collection and analysis, or in writing work.The authors thank Lima Soares Emanoella from Plant Genetics Laboratory of Gembloux Agro Bio-Tech, University of Liège for kindly revising the draft.
Balkunde R, Pesch M, Hülskamp M (2010) Trichome patterning in Arabidopsis thaliana: from genetic to molecular models. Curr Top Dev Biol 91:299–321
Chen Y, Chen B, Wang H, Hu W, Wang S, Zhou Z (2019) Combined elevated temperature and soil waterlogging stresses limit fibre biomass accumulation and fibre quality formation by disrupting protein activity during cotton fibre development. Funct Plant Biol 46(8):715–724
Chen W, Li Y, Zhu S, Fang S, Zhao L, Guo Y, Wang J, Yuan L, Lu Y, Liu F, Yao J, Zhang Y (2020) A retrotransposon insertion in GhMML3_D12 is likely responsible for the lintless locus li3 of tetraploid cotton. Front Plant Sci 11:593679. 10.3389/fpls.2020.593679 DOI: 10.3389/fpls.2020.593679
Cheng H, Lu C, John ZY, Zou C, Zhang Y, Wang Q, Huang J, Feng X, Jiang P, Yang W (2016) Fine mapping and candidate gene analysis of the dominant glandless gene Gl2e in cotton (Gossypium spp). Theor Appl Genet 129(7):1347–1355
Cheng G, Zhang L, Wei H, Wang H, Lu J, Yu S (2020) Transcriptome analysis reveals a gene expression pattern associated with fuzz fiber initiation induced by high temperature in Gossypium barbadense. Genes (basel) 11(9):1066
Dai X, Zhou L, Zhang W, Cai L, Guo H, Tian H, Schiefelbein J, Wang S (2016) A single amino acid substitution in the R3 domain of GLABRA1 leads to inhibition of trichome formation in Arabidopsis without affecting its interaction with GLABRA3. Plant Cell Environ 39(4):897–907
Di Cristina M, Sessa G, Dolan L, Linstead P, Baima S, Ruberti I, Morelli G (1996) The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J 10(3):393–402
Ding M, Jiang Y, Cao Y, Lin L, He S, Zhou W, Rong J (2014) Gene expression profile analysis of Ligon lintless-1 (Li1) mutant reveals important genes and pathways in cotton leaf and fiber development. Gene 535(2):273–285
Ding M, Cao Y, He S, Sun J, Dai H, Zhang H, Sun C, Jiang Y, Paterson AH, Rong J (2020) GaHD1, a candidate gene for the Gossypium arboreum SMA-4 mutant, promotes trichome and fiber initiation by cellular H2O2 and Ca2+ signals. Plant Mol Biol 103(4–5):409–423
Du X, Huang G, He S, Yang Z, Sun G, Ma X, Li N, Zhang X, Sun J, Liu M, Jia Y, Pan Z, Gong W, Liu Z, Zhu H, Ma L, Liu F, Yang D, Wang F, Fan W, Gong Q, Peng Z, Wang L, Wang X, Xu S, Shang H, Lu C, Zheng H, Huang S, Lin T, Zhu Y, Li F (2018) Resequencing of 243 diploid cotton accessions based on an updated A genome identifies the genetic basis of key agronomic traits. Nat Genet 50(6):796–802
Fang L, Gong H, Hu Y, Liu C, Zhou B, Huang T, Wang Y, Chen S, Fang DD, Du X (2017) Genomic insights into divergence and dual domestication of cultivated allotetraploid cottons. Genome Biol 18(1):33
Fang DD, Naoumkina M, Thyssen GN, Bechere E, Li P, Florane CB (2020) An EMS-induced mutation in a tetratricopeptide repeat-like superfamily protein gene (Ghir_A12G008870) on chromosome A12 is responsible for the li y short fiber phenotype in cotton. Theor Appl Genet 133(1):271–282
Feng X, Cheng H, Zuo D, Zhang Y, Wang Q, Liu K, Ashraf J, Yang Q, Li S, Chen X (2019) Fine mapping and identification of the fuzzless gene GaFzl in DPL972 (Gossypium arboreum). Theor Appl Genet 132(8):2169–2179
Gao Z, Sun W, Wang J, Zhao C, Zuo K (2019) GhbHLH18 negatively regulates fiber strength and length by enhancing lignin biosynthesis in cotton fibers. Plant Sci 286:7–16
Gilbert MK, Kim HJ, Tang Y, Naoumkina M, Fang DD (2014) Comparative transcriptome analysis of short fiber mutants Ligon-lintless 1 and 2 reveals common mechanisms pertinent to fiber elongation in cotton (Gossypium hirsutum L.). PLoS ONE 9(4):95554
He P, Zhang Y, Liu H, Yuan Y, Wang C, Yu J, Xiao G (2019) Comprehensive analysis of WOX genes uncovers that WOX13 is involved in phytohormone-mediated fiber development in cotton. BMC Plant Biol 19(1):312
Hinchliffe DJ, Turley RB, Naoumkina M, Kim HJ, Tang Y, Yeater KM, Li P, Fang DD (2011) A combined functional and structural genomics approach identified an EST-SSR marker with complete linkage to the Ligon lintless-2 genetic locus in cotton (Gossypium hirsutum L.). BMC Genom 12(1):445
Hu H, He X, Tu L, Zhu L, Zhu S, Ge Z, Zhang X (2016) GhJAZ2 negatively regulates cotton fiber initiation by interacting with the R2R3-MYB transcription factor GhMYB25-like. Plant J 88(6):921–935
Huang Y, Liu X, Tang K, Zuo K (2013) Functional analysis of the seed coat-specific gene GbMYB2 from cotton. Plant Physiol Biochem 73:16–22
Hülskamp M (2004) Plant trichomes: a model for cell differentiation. Nat Rev Mol Cell Biol 5(6):471–480
Ioannidi E, Rigas S, Tsitsekian D, Daras G, Alatzas A, Makris A, Tanou G, Argiriou A, Alexandrou D, Poethig S (2016) Trichome patterning control involves TTG1 interaction with SPL transcription factors. Plant Mol Biol 92(6):675–687
Jiang Y, Ding M, Cao Y, Yang F, Zhang H, He S, Dai H, Hao H, Rong J (2015) Genetic fine mapping and candidate gene analysis of the Gossypium hirsutum Ligon lintless-1 (Li1) mutant on chromosome 22 (D). Mol Genet Genomics 290(6):2199–2211
Kim HJ, Hinchliffe DJ, Triplett BA, Chen ZJ, Stelly DM, Yeater KM, Moon HS, Gilbert MK, Thyssen GN, Turley RB (2015) Phytohormonal networks promote differentiation of fiber initials on pre-anthesis cotton ovules grown in vitro and in planta. PLoS ONE 10(4):e0125046
Lee JJ, Woodward AW, Chen ZJ (2007) Gene expression changes and early events in cotton fibre development. Ann Bot 100(7):1391–1401
Liang W, Fang L, Xiang D, Hu Y, Feng H, Chang L, Zhang T (2015) Transcriptome analysis of short fiber mutant Ligon lintless-1 (Li1) reveals critical genes and key pathways in cotton fiber elongation and leaf development. PLoS ONE 10(11):e0143503
Liu B, Zhu Y, Zhang T (2015) The R3-MYB gene GhCPC negatively regulates cotton fiber elongation. PLoS ONE 10(2):e0116272
Liu X, Moncuquet P, Zhu Q-H, Stiller W, Zhang Z, Wilson I (2020) Genetic identification and transcriptome analysis of lintless and fuzzless traits in Gossypium arboreum L. Int J Mol Sci 21(5):1675
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408
Matías-Hernández L, Aguilar-Jaramillo AE, Cigliano RA, Sanseverino W, Pelaz S (2016) Flowering and trichome development share hormonal and transcription factor regulation. J Exp Bot 67(5):1209–1219
Mei G, Zhang Z (2019) Optimization of polar distribution of GhPIN3a in the ovule epidermis improves cotton fiber development. J Exp Bot 70(12):3021
Naoumkina M, Thyssen GN, Fang DD, Bechere E, Li P, Florane CB (2021a) Mapping-by-sequencing the locus of EMS-induced mutation responsible for tufted-fuzzless seed phenotype in cotton. Mol Genet Genomics 296(5):1041–1049
Naoumkina M, Thyssen GN, Fang DD, Li P, Florane CB (2021b) Elucidation of sequence polymorphism in fuzzless-seed cotton lines. Mol Genet Genomics 296(1):193–206
Ohashi Y, Oka A, Ruberti I, Morelli G, Aoyama T (2002) Entopically additive expression of GLABRA2 alters the frequency and spacing of trichome initiation. Plant J 29(3):359–369
Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G, Aoyama T (2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300(5624):1427–1430
Padmalatha KV, Patil DP, Kumar K, Dhandapani G, Kanakachari M, Phanindra ML, Kumar S, Mohan T, Jain N, Prakash AH (2012) Functional genomics of fuzzless-lintless mutant of Gossypium hirsutum L. cv. MCU5 reveal key genes and pathways involved in cotton fibre initiation and elongation. BMC Genom 13(1):624
Patel JD, Huang X, Lin L, Das S, Chandnani R, Khanal S, Adhikari J, Shehzad T, Guo H, Roy-Zokan EM (2020) The Ligon lintless-2 short fiber mutation is located within a terminal deletion of chromosome 18 in cotton. Plant Physiol 183(1):277–288
Pattanaik S, Patra B, Singh SK, Yuan L (2014) An overview of the gene regulatory network controlling trichome development in the model plant. Arabidopsis Front Plant Sci 5:259
Rerie WG, Feldmann KA, Marks MD (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Gene Dev 8(12):1388–1399
Rong J, Pierce GJ, Waghmare VN, Rogers CJ, Desai A, Chee PW, May OL, Gannaway JR, Wendel JF, Wilkins TA (2005) Genetic mapping and comparative analysis of seven mutants related to seed fiber development in cotton. Theor Appl Genet 111(6):1137–1146
Shan C, Shangguan X, Zhao B, Zhang X, Chao L, Yang C, Wang L, Zhu H, Zeng Y, Guo W (2014) Control of cotton fibre elongation by a homeodomain transcription factor GhHOX3. Nat Commun 5:5519
Sun R, Li C, Zhang J, Li F, Ma L, Tan Y, Wang Q, Zhang B (2017) Differential expression of microRNAs during fiber development between fuzzless-lintless mutant and its wild-type allotetraploid cotton. Sci Rep 7(1):3. 10.1038/s41598-017-00038-6 DOI: 10.1038/s41598-017-00038-6
Sun H, Hao P, Gu L, Cheng S, Wang H, Wu A, Ma L, Wei H, Yu S (2020a) Pectate lyase-like gene GhPEL76 regulates organ elongation in Arabidopsis and fiber elongation in cotton. Plant Sci 293:110395
Sun Q, Huang J, Guo Y, Yang M, Guo Y, Li J, Zhang J, Xu W (2020b) A cotton NAC domain transcription factor, GhFSN5, negatively regulates secondary cell wall biosynthesis and anther development in transgenic Arabidopsis. Plant Physiol Biochem 146:303–314
Thyssen GN, Fang DD, Turley RB, Florane CB, Li P, Mattison CP, Naoumkina M (2017) A Gly65Val substitution in an actin, GhACT_LI1, disrupts cell polarity and F-actin organization resulting in dwarf, lintless cotton plants. Plant J 90(1):111–121
Tian Y, Zhang T (2021) MIXTAs and phytohormones orchestrate cotton fiber development. Curr Opin Plant Biol 59:101975
Walford SA, Wu Y, Llewellyn DJ, Dennis ES (2012) Epidermal cell differentiation in cotton mediated by the homeodomain leucine zipper gene, GhHD-1. Plant J 71(3):464–478
Wan Q, Zhang H, Ye W, Wu H, Zhang T (2014) Genome-wide transcriptome profiling revealed cotton fuzz fiber development having a similar molecular model as Arabidopsis trichome. PLoS ONE 9(5):e97313
Wan Q, Guan X, Yang N, Wu H, Pan M, Liu B, Fang L, Yang S, Hu Y, Ye W (2016) Small interfering RNAs from bidirectional transcripts of GhMML3_A12 regulate cotton fiber development. New Phytol 210(4):1298–1310
Wang L, Zhu Y, Hu W, Zhang X, Cai C, Guo W (2015) Comparative transcriptomics reveals jasmonic acid-associated metabolism related to cotton fiber initiation. PLoS ONE 10(6):e0129854
Wang Y, Yu Y, Chen Q, Bai G, Gao W, Qu Y, Ni Z (2019) Heterologous expression of GbTCP4, a Class II TCP transcription factor, regulates trichome formation and root hair development in Arabidopsis. Genes 10(9):726
Wang L, Cheng H, Xiong F, Ma S, Zheng L, Song Y, Deng K, Wu H, Li F, Yang Z (2020a) Comparative phosphoproteomic analysis of BR-defective mutant reveals a key role of GhSK13 in regulating cotton fiber development. Sci China Life Sci 63(12):1905–1917
Wang L, Wang G, Long L, Altunok S, Feng Z, Wang D, Khawar KM, Mujtaba M (2020b) Understanding the role of phytohormones in cotton fiber development through omic approaches; recent advances and future directions. Int J Biol Macromol 163:1301–1313
Wang X, Miao Y, Cai Y, Sun G, Jia Y, Song S, Pan Z, Zhang Y, Wang L, Fu G, Gao Q, Ji G, Wang P, Chen B, Peng Z, Zhang X, Wang X, Ding Y, Hu D, Geng X, Wang L, Pang B, Gong W, He S, Du X (2020c) Large-fragment insertion activates gene GaFZ (Ga08G0121) and is associated with the fuzz and trichome reduction in cotton (Gossypium arboreum). Plant Biotechnol J 19(6):1110–1124
Wei Z, Li J (2018) Receptor-like protein kinases: Key regulators controlling root hair development in Arabidopsis thaliana. J Integr Plant Biol 60(9):841–850
Wu R, Citovsky V (2017a) Adaptor proteins GIR1 and GIR2. I. Interaction with the repressor GLABRA2 and regulation of root hair development. Biochem Biophys Res Commun 488(3):547–553
Wu R, Citovsky V (2017b) Adaptor proteins GIR1 and GIR2. II. Interaction with the co-repressor TOPLESS and promotion of histone deacetylation of target chromatin. Biochem Biophys Res Commun 488(4):609–613
Wu H, Tian Y, Wan Q, Fang L, Guan X, Chen J, Hu Y, Ye W, Zhang H, Guo W (2018) Genetics and evolution of MIXTA genes regulating cotton lint fiber development. New Phytol 217(2):883–895
Wu H, Zheng L, Qanmber G, Guo M, Wang Z, Yang Z (2021) Response of phytohormone mediated plant homeodomain (PHD) family to abiotic stress in upland cotton (Gossypium hirsutum spp.). BMC Plant Biol 21(1):13
Yang C, Ye Z (2013) Trichomes as models for studying plant cell differentiation. Cell Mol Life Sci 70(11):1937–1948
Yang C, Li H, Zhang J, Luo Z, Gong P, Zhang C, Li J, Wang T, Zhang Y, Ye Z (2011) A regulatory gene induces trichome formation and embryo lethality in tomato. Proc Natl Acad Sci USA 108(29):11836–11841
Zeng J, Zhang M, Hou L, Bai W, Yan X, Hou N, Wang H, Huang J, Zhao J, Pei Y (2019) Cytokinin inhibits cotton fiber initiation by disrupting PIN3a-mediated asymmetric accumulation of auxin in the ovule epidermis. J Exp Bot 70(12):3139–3151
Zhang G, Yue C, Lu T, Sun L, Hao F (2020) Genome-wide identification and expression analysis of NADPH oxidase genes in response to ABA and abiotic stresses, and in fibre formation in Gossypium. Peer J 8:e8404
Zhu J, Chen J, Gao F, Xu C, Wu H, Chen K, Si Z, Yan H, Zhang T (2017) Rapid mapping and cloning of the virescent-1 gene in cotton by bulked segregant analysis–next generation sequencing and virus-induced gene silencing strategies. J Exp Bot 68(15):4125–4135
Zhu Q, Yuan Y, Stiller W, Jia Y, Wang P, Pan Z, Du X, Llewellyn D, Wilson I (2018) Genetic dissection of the fuzzless seed trait in Gossypium barbadense. J Exp Bot 69(5):997–1009
Zhu Q, Stiller W, Moncuquet P, Gordon S, Yuan Y, Barnes S, Wilson I (2021) Genetic mapping and transcriptomic characterization of a new fuzzless-tufted cottonseed mutant. G3 (bethesda) 11(1):1–14