WUSCHEL-related Homeobox genes in Populus tomentosa: diversified expression patterns and a functional similarity in adventitious root formation

Springer Science and Business Media LLC - Tập 15 - Trang 1-14 - 2014
Bobin Liu1,2, Lin Wang2,3, Jin Zhang2, Jianbo Li2, Huanquan Zheng4, Jun Chen2,3, Mengzhu Lu1,2,3
1Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Nanjing Forestry University, Nanjing, China
2State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, China
3Key Laboratory of Non-wood Forest Product of State Forestry Administration, School of Forestry, Central South University of Forestry and Technology, Changsha, China
4Department of Biology, McGill University, Montreal, Canada

Tóm tắt

WUSCHEL (WUS)-related homeobox (WOX) protein family members play important roles in the maintenance and proliferation of the stem cell niche in the shoot apical meristem (SAM), root apical meristem (RAM), and cambium (CAM). Although the roles of some WOXs in meristematic cell regulation have been well studied in annual plants such as Arabidopsis and rice, the expression and function of WOX members in woody plant poplars has not been systematically investigated. Here, we present the identification and comprehensive analysis of the expression and function of WOXs in Populus tomentosa. A genome-wide survey identified 18 WOX encoding sequences in the sequenced genome of Populus trichocarpa (PtrWOXs). Phylogenetic and gene structure analysis revealed that these 18 PtrWOXs fall into modern/WUS, intermediate, and ancient clades, but that the WOX genes in P. trichocarpa may have expanded differently from the WOX genes in Arabidopsis. In the P. trichocarpa genome, no WOX members could be closely classified as AtWOX3, AtWOX6, AtWOX7, AtWOX10, and AtWOX14, but there were two copies of WOX genes that could be classified as PtrWUS, PtrWOX2, PtrWOX4, PtrWOX5, PtrWOX8/9, and PtrWOX11/12, and three copies of WOX genes that could be classified as PtrWOX1 and PtrWOX13. The use of primers specific for each PtrWOX gene allowed the identification and cloning of 18 WOX genes from P. tomentosa (PtoWOXs), a poplar species physiologically close to P. trichocarpa. It was found that PtoWOXs and PtrWOXs shared very high amino acid sequence identity, and that PtoWOXs could be classified identically to PtrWOXs. We revealed that the expression patterns of some PtoWOXs were different to their Arabidopsis counterparts. When PtoWOX5a and PtoWOX11/12a, as well as PtoWUSa and PtoWOX4a were ectopically expressed in transgenic hybrid poplars, the regeneration of adventitious root (AR) was promoted, indicating a functional similarity of these four WOXs in AR regeneration. This is the first attempt towards a systematical analysis of the function of WOXs in P. tomentosa. A diversified expression, yet functional similarity of PtoWOXs in AR regeneration is revealed. Our findings provide useful information for further elucidation of the functions and mechanisms of WOXs in the development of poplars.

Tài liệu tham khảo

Gehring WJ, Qian YQ, Billeter M, Furukubo-Tokunaga K, Schier AF, Resendez-Perez D, Affolter M, Otting G, Wüthrich K: Homeodomain-DNA recognition. Cell. 1994, 78: 211-223. 10.1016/0092-8674(94)90292-5. Garber R, Kuroiwa A, Gehring WJ: Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J. 1983, 2: 2027-2036. Gehring WJ: Exploring the homeobox. Gene. 1993, 135: 215-221. 10.1016/0378-1119(93)90068-E. Ariel FD, Manavella PA, Dezar CA, Chan RL: The true story of the HD-Zip family. Trends Plant Sci. 2007, 12: 419-426. 10.1016/j.tplants.2007.08.003. Vollbrecht E, Veit B, Sinha N, Hake S: The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature. 1991, 350: 241-243. 10.1038/350241a0. Van Der Graaff E, Laux T, Rensing SA: The WUS homeobox-containing (WOX) protein family. Genome Biol. 2009, 10: 248-10.1186/gb-2009-10-12-248. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T: Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development. 2004, 131: 657-668. 10.1242/dev.00963. Lin H, Niu L, McHale NA, Ohme-Takagi M, Mysore KS, Tadege M: Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants. Proc Natl Acad Sci. 2013, 110: 366-371. 10.1073/pnas.1215376110. Schoof H, Lenhard M, Haecker A, Mayer KFX, Jürgens G, Laux T: The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell. 2000, 100: 635-644. 10.1016/S0092-8674(00)80700-X. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T: Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature. 2007, 446: 811-814. 10.1038/nature05703. Stahl Y, Wink RH, Ingram GC, Simon R: A signaling module controlling the stem cell niche in Arabidopsis root meristem. Curr Biol. 2009, 19: 909-914. 10.1016/j.cub.2009.03.060. Hirakawa Y, Kondo Y, Fukuda H: TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell. 2010, 22: 2618-2629. 10.1105/tpc.110.076083. Suer S, Agusti J, Sanchez P, Schwarz M, Greb T: WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell. 2011, 23: 3247-3259. 10.1105/tpc.111.087874. Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T: Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell. 2008, 14: 867-876. 10.1016/j.devcel.2008.03.008. Shimizu R, Ji J, Kelsey E, Ohtsu K, Schnable PS, Scanlon MJ: Tissue specificity and evolution of meristematic WOX3 function. Plant Physiol. 2009, 149: 841-850. Park SO, Zheng Z, Oppenheimer DG, Hauser BA: The PRETTY FEW SEEDS2 gene encodes an Arabidopsis homeodomain protein that regulates ovule development. Development. 2005, 132: 841-849. 10.1242/dev.01654. Ji J, Shimizu R, Sinha N, Scanlon MJ: Analyses of WOX4 transgenics provide further evidence for the evolution of the WOX gene family during the regulation of diverse stem cell functions. Plant Signal Behav. 2010, 5: 916-920. 10.4161/psb.5.7.12104. Palovaara J, Hallberg H, Stasolla C, Hakman I: Comparative expression pattern analysis of WUSCHEL-related homeobox 2 (WOX2) and WOX8/9 in developing seeds and somatic embryos of the gymnosperm Picea abies. New Phytol. 2010, 188: 122-135. 10.1111/j.1469-8137.2010.03336.x. Wu X, Dabi T, Weigel D: Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr Biol. 2005, 15: 436-440. 10.1016/j.cub.2004.12.079. Zhao Y, Hu Y, Dai M, Huang L, Zhou DX: The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell. 2009, 21: 736-748. 10.1105/tpc.108.061655. Romera-Branchat M, Ripoll JJ, Yanofsky MF, Pelaz S: The WOX13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit. Plant J. 2013, 73: 37-49. 10.1111/tpj.12010. Deveaux Y, Toffano-Nioche C, Claisse G, Thareau V, Morin H, Laufs P, Moreau H, Kreis M, Lecharny A: Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evol Biol. 2008, 8: 291-10.1186/1471-2148-8-291. Etchells JP, Provost CM, Mishra L, Turner SR: WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation. Development. 2013, 140: 2224-2234. 10.1242/dev.091314. Demura T, Ye ZH: Regulation of plant biomass production. Curr Opin Plant Biol. 2010, 13: 298-303. 10.1016/j.pbi.2010.03.002. Nieminen K, Robischon M, Immanen J, Helariutta Y: Towards optimizing wood development in bioenergy trees. New Phytol. 2012, 194: 46-53. 10.1111/j.1469-8137.2011.04011.x. Slavov GT, DiFazio SP, Martin J, Schackwitz W, Muchero W, Rodgers-Melnick E, Lipphardt MF, Pennacchio CP, Hellsten U, Pennacchio LA, Gunter LE, Ranjan P, Vining K, Pomraning KR, Wilhelm LJ, Pellegrini M, Mockler TC, Freitag M, Geraldes A, El-Kassaby YA, Mansfield SD, Cronk QCB, Douglas CJ, Strauss SH, Rokhsar D, Tuskan GA: Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytol. 2012, 196: 713-725. 10.1111/j.1469-8137.2012.04258.x. Zhang X, Zong J, Liu J, Yin J, Zhang D: Genome-wide analysis of WOX gene family in rice, sorghum, maize, arabidopsis and poplar. J Integr Plant Biol. 2010, 52: 1016-1026. 10.1111/j.1744-7909.2010.00982.x. Gambino G, Minuto M, Boccacci P, Perrone I, Vallania R, Gribaudo I: Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis vinifera. J Exp Bot. 2010, 62: 1089-1101. Nardmann J, Reisewitz P, Werr W: Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Mol Bio Evol. 2009, 26: 1745-1755. 10.1093/molbev/msp084. Hedman H, Zhu T, von Arnold S, Sohlberg JJ: Analysis of the WUSCHEL-RELATED HOMEOBOX gene family in the conifer picea abies reveals extensive conservation as well as dynamic patterns. BMC Plant Biol. 2013, 13: 89-10.1186/1471-2229-13-89. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, et al: The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science. 2006, 313: 1596-1604. 10.1126/science.1128691. Mayer KFX, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T: Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell. 1998, 95: 805-815. 10.1016/S0092-8674(00)81703-1. Nakata M, Matsumoto N, Tsugeki R, Rikirsch E, Laux T, Okada K: Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell. 2012, 24: 519-535. 10.1105/tpc.111.092858. Wu X, Chory J, Weigel D: Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Dev Biol. 2007, 309: 306-316. 10.1016/j.ydbio.2007.07.019. Matsumoto N, Okada K: A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev. 2001, 15: 3355-3364. 10.1101/gad.931001. Cheng ZJ, Wang L, Sun W, Zhang Y, Zhou C, Su YH, Li W, Sun TT, Zhao XY, Li XG, Cheng Y, Zhao Y, Xie Q, Zhang XS: Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3. Plant Physiol. 2012, 161: 240-251. Nardmann J, Ji J, Werr W, Scanlon MJ: The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development. 2004, 131: 2827-2839. 10.1242/dev.01164. Ji J, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ: WOX4 promotes procambial development. Plant Physiol. 2009, 152: 1346-1356. Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, Ohashi-Ito K, Matsubayashi Y, Fukuda H: Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci. 2008, 105: 15208-15213. 10.1073/pnas.0808444105. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25: 4876-4882. 10.1093/nar/25.24.4876. Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003, 52: 696-704. 10.1080/10635150390235520. Jones DT, Taylor WR, Thornton JM: The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992, 8: 275-282. Guo AY, Zhu QH, Chen X, Luo JC: GSDS: a gene structure display server. Yi Chuan. 2007, 29: 1023-1026. 10.1360/yc-007-1023. Bailey TL, Williams N, Misleh C, Li WW: MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006, 34: 369-373.