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Journal of Integrative Agriculture  2019, Vol. 18 Issue (2): 361-371    DOI: 10.1016/S2095-3119(18)61914-8
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Up-regulation of a homeodomain-leucine zipper gene HD-1 contributes to trichome initiation and development in cotton
NIU Er-li, CAI Cai-ping, BAO Jiang-hao, WU Shuang, ZHAO Liang, GUO Wang-zhen
State Key Laboratory of Crop Genetics & Germplasm Enhancement, Ministry of Science and Technology/Hybrid Cotton R&D Engineering Research Center, Ministry of Education/College of Agriculture, Nanjing Agricultural University, Nanjing 210095, P.R.China
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Abstract  
Plant trichomes originate from epidermal cells.  In this work, we demonstrated that a homeodomain-leucine zipper (HD-Zip) gene, Gh_A06G1283 (GhHD-1A), was related to the leaf trichome trait in allotetraploid cotton and could be a candidate gene for the T1 locus.  The ortholog of GhHD-1A  in the hairless accession Gossypium barbadense cv. Hai7124 was interrupted by a long terminal repeat (LTR) retrotransposon, while GhHD-1A worked well in the hairy accession Gossypium hirsutum acc. T586.  Sequence and phylogenetic analysis showed that GhHD-1A  belonged to the HD-Zip IV gene family, which mainly regulated epidermis hair development in plants.  Silencing of GhHD-1A  and its homoeologs GhHD-1D in allotetraploid T586 and Hai7124 could significantly reduce the density of leaf hairs and affect the expression levels of other genes related to leaf trichome formation.  Further analysis found that GhHD-1A  mainly regulated trichome initiation on the upper epidermal hairs of leaves in cotton, while the up-regulated expression of GhHD-1A  in different organs/tissues also altered epidermal trichome development.  This study not only helps to unravel the important roles of GhHD-1A  in regulating trichome initiation in cotton, but also provides a reference for exploring the different forms of trichome development in plants.
Keywords:  leaf trichome        map-based cloning       a homeodomain-leucine zipper gene HD-1        virus-induced gene silencing (VIGS)        functional differentiation  
Received: 21 December 2017   Accepted:
Fund: This work was supported by the National Natural Science Foundation of China (31471539) and the Jiangsu Collaborative Innovation Center for Modern Crop Production Project, China (No.10).
Corresponding Authors:  Correspondence GUO Wang-zhen, Tel: +86-25-84396523, E-mail: moelab@njau.edu.cn   
About author:  NIU Er-li, E-mail: niuerli@zaas.ac.cn;

Cite this article: 

NIU Er-li, CAI Cai-ping, BAO Jiang-hao, WU Shuang, ZHAO Liang, GUO Wang-zhen. 2019. Up-regulation of a homeodomain-leucine zipper gene HD-1 contributes to trichome initiation and development in cotton. Journal of Integrative Agriculture, 18(2): 361-371.

Balkunde R, Pesch M, Hulskamp M. 2010. Trichome patterning in Arabidopsis thaliana from genetic to molecular models. Current Topics in Developmental Biology, 91, 299–321.
Basara A S, Malik C P. 1984. Development of cotton fiber. International Review of Cytology, 89, 65–113.
Chang L, Fang L, Zhu Y, Wu H, Zhang Z, Liu C, Li X, Zhang T. 2016. Insights into interspecific hybridization events in allotetraploid cotton formation from characterization of a gene-regulating leaf shape. Genetics, 204, 799–806.
Ciarbelli A R, Ciolfi A, Salvucci S, Ruzza V, Possenti M, Carabelli M, Fruscalzo A, Sessa G, Morelli G, Ruberti I. 2008. The Arabidopsis homeodomain-leucine Zipper II gene family: Diversity and redundancy. Plant Molecular Biology, 68, 465–478.
Ding M, Ye W, Lin L, He S, Du X, Chen A, Cao Y, Qin Y, Yang F, Jiang Y, Zhang H, Wang X, Paterson A H, Rong J. 2015. The hairless stem phenotype of cotton (Gossypium barbadense) is linked to a copia-like retrotransposon insertion in a homeodomain-leucine zipper gene (HD1). Genetics, 201, 143–154.
Finn R D, Clements J, Eddy S R. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Research, 39, W29–W37.
Finn R D, Coggill P, Eberhardt R Y, Eddy S R, Mistry J, Mitchell A L, Potter S C, Punta M, Qureshi M, Sangrador-Vegas A, Salazar G A, Tate J, Bateman A. 2016. The Pfam protein families database: Towards a more sustainable future. Nucleic Acids Research, 44, D279–D285.
Guan X Y, Li Q J, Shan C M, Wang S, Mao Y B, Wang L J, Chen X Y. 2008. The HD-Zip IV gene GaHOX1 from cotton is a functional homologue of the Arabidopsis GLABRA2. Plant Physiology, 134, 174–182.
Guo W, Cai C, Wang C, Han Z, Song X, Wang K, Niu X, Wang C, Lu K, Shi B, Zhang T. 2007. A microsatellite-based, gene-rich linkage map reveals genome structure, function and evolution in Gossypium. Genetics, 176, 527–541.
Guo W Z, Ma G J, Zhu Y C, Yi C X, Zhang T Z. 2006. Molecular tagging and mapping of quantitative trait loci for lint percentage and morphological marker genes in Upland cotton. Journal of Integrative Plant Biology, 48, 320–326.
Henriksson E, Olsson A S, Johannesson H, Johansson H, Hanson J, Engström P, Söderman E. 2005. Homeodomain leucine zipper class I genes in Arabidopsis expression patterns and phylogenetic relationships. Plant Physiology, 139, 509–518.
Hu B, Jin J, Guo A Y, Zhang H, Luo J, Gao G. 2015. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics, 31, 1296–1297.
Hulskamp M, Misera S, Jurgens G. 1994. Genetic dissection of trichome cell development in Arabidopsis. Cell, 76, 555–566.
Humphries J A, Walker A R, Timmis J N, Orford S J. 2005. Two WD-repeat genes from cotton are functional homologues of the Arabidopsis thaliana TRANSPARENT TESTA GLABRA1 (TTG1) gene. Plant Molecular Biology, 57, 67–81.
Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, Hayashi H, Shibata D, Sato S, Kato T, Tabata S, Okada K, Wada T. 2007. Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. The Plant Cell, 19, 2531–2543.
Jiang Y, Guo W, Zhu H, Ruan Y, Zhang T. 2012. Overexpression of GhSusA1 increases plant biomass and improves cotton fiber yield and quality. Plant Biotechnology Journal, 10, 301–312.
Kohel R J, Leuis C F. 1984. Cotton. American Society of Agronomy Publishers. Madison, Wisconsin.
Lacape J M, Nguyen T B. 2005. Mapping quantitative trait loci associated with leaf and stem pubescence in cotton. Journal of Heredity, 96, 441–444.
Lee J A. 1985. Revision of the genetics of the hairiness-smoothness system of Gossypium. Journal of Heredity, 76, 123–126.
Lee J A. 1968. Genetical studies concerning the distribution of trichomes on the leaves of GOSSYPIUM HIRSUTUM L. Genetics, 60, 567–575.
Li F, Fan G, Wang K, Sun F, Yuan Y, Song G, Li Q, Ma Z, Lu C, Zou C, Chen W, Liang X, Shang H, Liu W, Shi C, Xiao G, Gou C, Ye W, Xu X, Zhang X, et al. 2014. Genome sequence of the cultivated cotton Gossypium arboreum. Nature Genetics, 46, 567–572.
Li F, Fan G, Lu C, Xiao G, Zou C, Kohel R J, Ma Z, Shang H, Ma X, Wu J, Liang X, Huang G, Percy R G, Liu K, Yang W, Chen W, Du X, Shi C, Yuan Y, Ye W, et al. 2015. Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nature Biotechnology, 33, 524–530.
Liu X, Zhao B, Zheng H, Hu Y, Lu G, Yang C Q, Chen J D, Chen J J, Chen D Y, Zhang L, Zhou Y, Wang L J, Guo W Z, Bai Y L, Ruan J X, Shangguan X X, Mao Y B, Shan C M, Jiang J P, Zhu Y Q, et al. 2015. Gossypium barbadense genome sequence provides insight into the evolution of extra-long staple fiber and specialized metabolites. Scientific Reports, 5, 14139.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–??CT method. Methods, 25, 402–408.
Lu P, Porat R, Nadeau J A, O’Neill S D. 1996. Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. The Plant Cell, 8, 2155–2168.
Ma D, Hu Y, Yang C, Liu B, Fang L, Wan Q, Liang W, Mei G, Wang L, Wang H, Ding L, Dong C, Pan M, Chen J, Wang S, Chen S, Cai C, Zhu X, Guan X, Zhou B, et al. 2016. Genetic basis for glandular trichome formation in cotton. Nature Communications, 7, 10456.
Meredith W R, Pettigrew W T, Heitholt J J. 1996. Subokra, semi-smoothness and nectariless effect on cotton lint yield. Crop Science, 36, 22–25.
Nakamura M, Katsumata H, Abe M, Yabe N, Komeda Y, Yamamoto K T, Takahashi T. 2006. Characterization of the class IV homeodomain-leucine zipper gene family in Arabidopsis. Plant Physiology, 141, 1363–1375.
Niu E, Shang X, Cheng C, Bao J, Zeng Y, Cai C, Du X, Guo W. 2015. Comprehensive analysis of the COBRA-Like (COBL) gene family in Gossypium identifies two COBLs potentially associated with fiber quality. PLoS ONE, 10, e0145725.
Van Ooijen J W, Voorrips R E. 2001. JoinMap version 3.0: Software for the calculation of genetic linkage maps. In: International Journal of Plant Research. Wageningen, The Netherlands. pp. 1–51.
Paterson A H, Brubaker C L, Wendel J F. 1993. A rapid method for extraction of cotton (Gossypium spp.) genomic DNA suitable for RFLP or PCR analysis. Plant Molecular Biology Reporter, 11, 122–127.
Paterson A H, Wendel J F, Gundlach H, Guo H, Jenkins J, Jin D, Llewellyn D, Showmaker K C, Shu S, Udall J, Yoo M J, Byers R, Chen W, Doron-Faigenboim A, Duke M V, Gong L, Grimwood J, Grover C, Grupp K, Hu G, et al. 2012. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature, 492, 423–427.
Shan C M, Shangguan X X, Zhao B, Zhang X F, Chao L M, Yang C Q, Wang L J, Zhu H Y, Zeng Y D, Guo W Z, Zhou B L, Hu G J, Guan X Y, Chen Z J, Wendel J F, Zhang T Z, Chen X Y. 2014. Control of cotton ?bre elongation by a homeodomain transcription factor GhHOX3. Nature Communications, 5, 5519.
Szymanski D B, Jilk R A, Pollock S M, Marks M D. 1998. Control of GL2 expression in Arabidopsis leaves and trichomes. Development, 125, 1161–1171.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.
Thomson N J, Reid P E, Williams E R. 1987. Effects of the okra leaf, nectariless, frego bract and glabrous conditions on yield and quality of cotton lines. Euphytica, 36, 545–553.
Voorrips R E. 2002. MapChart: Software for the graphical presentation of linkage maps and QTLs. Journal of Heredity, 93, 77–78.
Walford S A, Wu Y, Llewellyn D J, Dennis E S. 2012. Epidermal cell differentiation in cotton mediated by the homeodomain leucine zipper gene, GhHD-1. The Plant Journal, 71, 464–478.
Wan Q, Zhang Z, Hu M, Chen L, Liu D, Chen X, Wang W, Zheng J. 2007. T1 locus in cotton is the candidate gene affecting lint percentage, fiber quality and spiny bollworm (Earias spp.) resistance. Euphytica, 158, 241–247.
Wang S, Wang J W, Yu N, Li C H, Luo B, Gou J Y, Wang L J, Chen X Y. 2004. Control of plant trichome development by a cotton fiber MYB gene. The Plant Cell, 16, 2323–2334.
Werker E. 2000. Trichome diversity and development. In: Hallahan D L, Gray J C, eds., Advances in Botanical Research. Plant Trichomes. Academic Press, New York. pp. 1–35.
Wright R J, Thaxton P M, El-Zik K M, Paterson A H. 1999. Molecular mapping of genes affecting pubescence of cotton. Journal of Heredity, 90, 215–219.
Xu Z, Wang H. 2007. LTR_FINDER: An efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Research, 35, W265–W268.
Zapata L, Ding J, Willing EM, Hartwig B, Bezdan D, Jiao W B, Patel V, Velikkakam James G, Koornneef M, Ossowski S, Schneeberger K. 2016. Chromosome-level assembly of Arabidopsis thaliana Ler reveals the extent of translocation and inversion polymorphisms. Proceedings of the National Academy of Sciences of the United States of America, 113, E4052–E4060.
Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski C A, Scheffler B E, Stelly D M, Hulse-Kemp A M, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, et al. 2015. Sequencing of allotetraploid cotton (Gossypium hirsutum acc. TM-1) provides a resource for fiber improvement. Nature Biotechnology, 33, 531–537.
Zhu Q H, Zhang J, Liu D, Stiller W, Liu D, Zhang Z, Llewellyn D, Wilson I. 2016. Integrated mapping and characterization of the gene underlying the okra leaf trait in Gossypium hirsutum L. Journal of Experimental Botany, 67, 763–774.
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