Abstract
WUSCHEL-related homeobox (WOX) gene family has important role in plant developmental process and represents a class of plant specific transcription factors that are involved in early phase of embryogenesis by coordinating gene transcription. Recent available pineapple whole genome sequences provide a base for detail comprehensive phylogenetic analysis of the WOX genes in pineapple. Ten WOX genes were found in pineapple genome and were located on 6 chromosomes. On the basis of phylogenetic analysis, WOX gene family was divided into three clades and structural analysis revealed that WOX gene family is highly conserved in pineapple. Gene structure analysis revealed that five genes had two exons with only one intron. Expression profiles based on RNA-Seq of different tissues revealed seven genes showed very low expression in almost all tissues (leaf, flower, root, fruit, stamen, sepal, petal and ovule) at all developmental stages. AcoWOX13 exhibited relatively higher expression in all tissues while the highest expression was shown by AcoWUS at ovule stage 1. Expression analysis under abiotic stresses analyzed by qRT-PCR, showed a dynamic response of WOX genes to abiotic stresses. Interestingly qRT-PCR had result pattern similar to RNA-Seq data as AcoWOX13 had high expression for all abiotic stresses while other WOX genes were down-regulated. This is the first genome-wide study of the WOX genes in pineapple coupled with high throughput RNA-seq for the identification, structural and functional analysis of 10 WOX genes in pineapple. Our study provides more insight for future studies regarding the functions of WOX genes in pineapple.
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Abbreviations
- WOX:
-
WUSCHEL-related homeobox
- RNA-Seq:
-
RNA sequencing
- qRT-PCR:
-
quantitative real-time PCR
- WUS:
-
Wuschel
- NaCl:
-
sodium chloride
References
Baena-González E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13:474–482
Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942
Bharathan G, Janssen BJ, Kellogg EA, Sinha N (1997) Did homeodomain proteins duplicate before the origin of angiosperms, fungi, and metazoa? Proc Natl Acad Sci U S A 94:13749–13753
Bhattacharjee A, Ghangal R, Garg R, Jain M (2015) Genome-wide analysis of homeobox gene family in legumes: identification, gene duplication and expression profiling. PLoS One 10:e0119198
Bray EA, Bailey-serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Biologists, Rockville, pp 1158–1203
Buscaill P, Rivas S (2014) Transcriptional control of plant defence responses. Curr Opin Plant Biol 20:35–46
Cai H, Cheng J, Yan Y, Xiao Z, Li J et al (2015) Genome-wide identification and expression analysis of calcium-dependent protein kinase and its closely related kinase genes in Capsicum Annuum. Front Plant Sci 6:737
Cai H, Zhao L, Wang L, Zhang M, Su Z, et al (2017) ERECTA signaling controls Arabidopsis inflorescence architecture through chromatin-mediated activation of PRE1 expression. New Phytol 214:1579–1596
Chen C, Zhang Y, Xu Z, Luan A, Mao Q, et al (2016) Transcriptome profiling of the pineapple under low temperature to facilitate its breeding for cold tolerance (J.-H. Liu, Ed.). PLoS One 11: e0163315
Chinnusamy V, Schumaker K, Zhu J-K (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236
Deveaux Y, Toffano-Nioche C, Claisse G, Thareau V, Morin H et al (2008) Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evol Biol 8:291
Gambino G, Minuto M, Boccacci P, Perrone I, Vallania R et al (2011) Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis Vinifera. J Exp Bot 62:1089–1101
Ge Y, Liu J, Zeng M, He J, Qin P et al (2016) Identification of WOX family genes in Selaginella Kraussiana for studies on stem cells and regeneration in Lycophytes. Front Plant Sci 7:93
Gehring WJ (1987) Homeo boxes in the study of development. Science 236:1245–1252
Gehring WJ (1993) Exploring the homeobox. Gene 135:215–221
Gehring WJ, Affolter M, Burglin T (1994) Homeodomain Proteins. Annu Rev Biochem 63:487–526
Guo A-Y, Zhu Q-H, Gu X, Ge S, Yang J et al (2008) Genome-wide identification and evolutionary analysis of the plant specific SBP-box transcription factor family. Gene 418:1–8
Haecker A, Groß-Hardt R, Geiges B, Sarkar A, Breuninger H et al (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis Thaliana. Development 131:657–668
Kamiya N, Nagasaki H, Morikami A, Sato Y, Matsuoka M (2003) Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J 35:429–441
Lata C, Yadav A, Pras M (2011) Role of plant transcription factors in abiotic stress tolerance. Ine: Abiotic stress response in plants - physiological, biochemical and genetic perspectives. InTech
Laux T, Mayer KF, Berger J, Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96
Li X, Duan X, Jiang H, Sun Y, Tang Y et al (2006) Genome-wide analysis of basic/helix-loop-helix transcription factor family in Rice and Arabidopsis. Plant Physiol 141:1167–1184
Lian G, Ding Z, Wang Q, Zhang D, Xu J (2014) Origins and evolution of WUSCHEL-related homeobox protein family in plant kingdom. ScientificWorldJournal 2014:534140
Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18:1509–1517
Matsumoto N, Okada K (2001) A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev 15:3355–3364
Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G et al (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815
Ming R, VanBuren R, Wai CM, Tang H, Schatz MC et al (2015) The pineapple genome and the evolution of CAM photosynthesis. Nat Genet 47:1435–1442
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628
Nardmann J, Ji J, Werr W, Scanlon MJ (2004) The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131:2827–2839
Nardmann J, Zimmermann R, Durantini D, Kranz E, Werr W (2007) WOX gene phylogeny in Poaceae: a comparative approach addressing leaf and embryo development. Mol Biol Evol 24:2474–2484
Nardmann J, Reisewitz P, Werr W (2009) Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Mol Biol Evol 26:1745–1755
Park SO, Zheng Z, Oppenheimer DG, Hauser BA (2005) The PRETTY FEW SEEDS2 gene encodes an Arabidopsis homeodomain protein that regulates ovule development. Development 132:841–849
Redwan RM, Saidin A, Kumar SV (2016) The draft genome of MD-2 pineapple using hybrid error correction of long reads. DNA Res 23:427–439
Riechmann JL, Heard J, Martin G, Reuber L, Jiang C et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110
Rushton PJ, Somssich IE (1998) Transcriptional control of plant genes responsive to pathogens. Curr Opin Plant Biol 1:311–315
Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T et al (2007) Conserved factors regulate signalling in Arabidopsis Thaliana shoot and root stem cell organizers. Nature 446:811–814
Singh K, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436
Smith LB (1979) (Bromeliaceae) 3. Bromelioideae. Hafner, New York
Su Z, Wang L, Li W, Zhao L, Huang X, et al (2017) Genome-wide identification of auxin response factor (ARF) genes family and its tissue-specific prominent expression in pineapple (Ananas comosus). Trop Plant Biol 10:86–96
Suer S, Agusti J, Sanchez P, Schwarz M, Greb T (2011) WOX4 imparts Auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23:3247–3259
Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43
Trapnell C, Roberts A, Goff L, Pertea G, Kim D et al (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and cufflinks. Nat Protoc 7:562–578
van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10:248
Vandenbussche M, Horstman A, Zethof J, Koes R, Rijpkema AS et al (2009) Differential recruitment of WOX transcription factors for lateral development and organ fusion in petunia and Arabidopsis. Plant Cell Online 21:2269–2283
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63
Wolberger C (1996) Homeodomain interactions. Curr Opin Struct Biol 6:62–68
Wu X, Dabi T, Weigel D (2005) Requirement of Homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr Biol 15:436–440
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803
Yamaguchi-Shinozaki K, Kasuga M, Liu Q, Miura S, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291
Zhang X, Zong J, Liu J, Yin J, Zhang D (2010) Genome-wide analysis of WOX gene family in Rice, sorghum, maize, Arabidopsis and poplar. J Integr Plant Biol 52:1016–1026
Acknowledgments
This work was supported by NSFC (31522009; 31470284; U1605212 to Y.Q.), Fujian Innovative Center for Germplasm Resources and Innovation project of Characteristic Horticultural Crop Seed Industry (KLA15001D), FAFU international collaboration project and Natural Science Foundation of Fujian Province (2017 J01601).
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Communicated by: Hongwei Cai
Syed Muhammad Azam and Yanhui Liu are co-author
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Rahman, Z.u., Azam, S.M., Liu, Y. et al. Expression Profiles of Wuschel-Related Homeobox Gene Family in Pineapple (Ananas comosus L). Tropical Plant Biol. 10, 204–215 (2017). https://doi.org/10.1007/s12042-017-9192-9
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DOI: https://doi.org/10.1007/s12042-017-9192-9