Transcriptome profiling reveals roles of meristem regulators and polarity genes during fruit trichome development in cucumber (Cucumis sativus L.)

Journal of Experimental Botany

Volumn 65, Issue 17, 2014, Pages 4943-4958

  Chen, Chunhua ^a   Liu, Meiling ^a   Jiang, Li ^a   Liu, Xiaofeng ^a   Zhao, Jianyu ^a   Yan, Shuangshuang ^a   Yang, Sen ^a   Ren, Huazhong ^a   Liu, Renyi ^b   Zhang, Xiaolan ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cucumber; Fruit spine; Meristem regulator; Polarity transcriptome; Trichome

Indexed keywords

TRANSCRIPTOME; VEGETABLE PROTEIN;

CUCUMBER; FRUIT; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; MUTATION; TRICHOME;

CUCUMIS SATIVUS; FRUIT; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; MERISTEM; MUTATION; PLANT PROTEINS; TRANSCRIPTOME; TRICHOMES;

CUCUMIS SATIVUS;

EID: 84907387075     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru258     Document Type: Article

References (73)

1. Alexa A, Rahnenfuhrer J, Lengauer T. 2006. Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22, 1600-1607.
2. Ando K, Carr KM, Grumet R. 2012. Transcriptome analyses of early cucumber fruit growth identifies distinct gene modules associated with phases of development. BMC Genomics 518, 1471-2164.
3. Benjamini Y, and Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B 57, 289-300.
4. Bharathan G, Goliber TE, Moore C, Kessler S, Pham T, Sinha NR. 2002. Homologies in leaf form inferred from KNOXI gene expression during development. Science 296, 1858-1860.
5. Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA. 2000. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408, 967-971.
6. Byrne ME, Simorowski J, Martienssen RA. 2002. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129, 1957-1965.
7. Chien JC, Sussex IM. 1996. Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L.) Heynh. Plant Physiology 111, 1321-1328.
8. Churchman ML, Brown ML, Kato N, et al. 2006. SIAMESE, a plantspecific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell 18, 3145-3157.
9. Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM. 1996. The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122, 1567-1575.
10. Daimon Y, Takabe K, Tasaka M. 2003. The CUP-SHAPED COTYLEDON genes promote adventitious shoot formation on calli. Plant and Cell Physiology 44, 113-121.
11. Deng W, Yang Y, Ren Z, Audran-Delalande C, Mila I, Wang X, Song H, Hu Y, Bouzayen M, Li Z. 2012. The tomato SlIAA15 is involved in trichome formation and axillary shoot development. New Phytologist 194, 379-390.
12. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL. 2003. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Current Biology 13, 1768-1774.
13. Esch JJ, Chen MA, Hillestad M, Marks MD. 2004. Comparison of TRY and the closely related At1g01380 gene in controlling Arabidopsis trichome patterning. The Plant Journal 40, 860-869.
14. Eshed Y, Baum SF, Perea JV, Bowman JL. 2001. Establishment of polarity in lateral organs of plants. Current Biology 11, 1251-1260.
15. Eveland AL, Satoh-Nagasawa N, Goldshmidt A, Meyer S, Beatty M, Sakai H, Ware D, Jackson D. 2010. Digital gene expression signatures for maize development. Plant Physiology 154, 1024-1039.
16. Fletcher JC. 2002. Shoot and floral meristem maintenance in arabidopsis. Annual Review of Plant Biology 53, 45-66.
17. Galbraith DW, Lambert GM, Macas J, Dolezel J. 2001. Analysis of nuclear DNA content and ploidy in higher plants. Curr Protoc Cytom Chapter 7, Unit 7.6.
18. Galway ME, Masucci JD, Lloyd AM, Walbot V, Davis RWSJW. 1994. The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Developmental Biology 166, 740-754.
19. Hake S, Smith HM, Holtan H, Magnani E, Mele G, Ramirez J. 2004. The role of knox genes in plant development. Annual Review of Cell and Developmental Biology 20, 125-151.
20. Hibara K, Karim MR, Takada S, Taoka K, Furutani M, Aida M, Tasaka M. 2006. Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18, 2946-2957.
21. Huang S, Li R, Zhang Z, et al. 2009. The genome of the cucumber, Cucumis sativus L. Nature Genetics 41, 1275-1281.
22. Hülskamp M. 2004. Plant trichomes: a model for cell differentiation. Nature Reviews Molecular Cell Biology 5, 471-480.
23. Hülskamp M, Miséra S, Jürgens G. 1994. Genetic dissection of trichome cell development in Arabidopsis. Cell 76, 555-566.
24. Hülskamp M, Schnittger A, Folkers U. 1999. Pattern formation and cell differentiation: trichomes in Arabidopsis as a genetic model system. Int Rev Cytol 186, 147-178.
25. Hülskamp M, Schnittger A. 1998. Spatial regulation of trichome formation in Arabidopsis thaliana. Seminars in Cell and Developmental Biology 9, 213-220.
26. Jacobsen SE, Binkowski KA, Olszewski NE. 1996. SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proceedings of the National Academy of Sciences, USA 93, 9292-9296.
27. Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC. 2004. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428, 84-88.
28. Kang JH, Shi F, Jones AD, Marks MD, Howe GA. 2010. Distortion of trichome morphology by the hairless mutation of tomato affects leaf surface chemistry. Journal of Experimental Botany 61, 1053-1064.
29. Kirik V, Simon M, Huelskamp M, Schiefelbein J. 2004a. The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Developmental Biology 268, 506-513.
30. Kirik V, Simon M, Wester K, Schiefelbein J, Hülskamp M. 2004b. ENHANCER of TRY and CPC 2 (ETC2) reveals redundancy in the regionspecic control of trichome development of Arabidopsis. Plant Molecular Biology 55, 389-398.
31. Larkin JC, Brown ML, Schiefelbein J. 2003. How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annual Review of Plant Biology 54, 403-430.
32. Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA. 2004. The tomato homolog of CORONATINEINSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16, 126-143.
33. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J. 2009. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966-1967.
34. Long JA, Moan EI, Medford JI, Barton MK. 1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66-69.
35. Luckwill LC. 1943. The genus Lycopersicon: a historical, biological and taxonomic survey of the wild and cultivated tomato. Aberd Univ Stud 120, 1-44.
36. Machado A, Wu Y, Yang Y, Llewellyn DJ, Dennis ES. 2009. The MYB transcription factor GhMYB25 regulates early fibre and trichome development. The Plant Journal 59, 52-62.
37. Marks MD. 1997. Molecular genetic analysis of trichome development in Arabidopsis. Annual Review of Plant Physiology and Plant Molecular Biology 48, 137-163.
38. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK. 2001. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411, 709-713.
39. Melaragno JE, Mehrotra B, Coleman AW. 1993. Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5, 1661-1668.
40. Nakata M, Okada K. 2012. The three-domain model: a new model for the early development of leaves in Arabidopsis thaliana. Plant Signaling & Behavior 7, 1423-1427.
41. Oppenheimer DG, Herman PL, Sivakumaran S, Esch J, Marks MD. 1991. A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67, 483-493.
42. Ori N, Eshed Y, Chuck G, Bowman JL, Hake S. 2000. Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127, 5523-5532.
43. Otsuga D, DeGuzman B, Prigge MJ, Drews GN, Clark SE. 2001. REVOLUTA regulates meristem initiation at lateral positions. The Plant Journal 25, 223-236.
44. Payne CT, Zhang F, Lloyd AM. 2000. GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156, 1349-1362.
45. Perazza D, Herzog M, Hülskamp M, Brown S, Dorne A-M, Bonneville J-M. 1999. Trichome cell growth in Arabidopsis thaliana can be derepressed by mutations in at least five genes. Genetics 152, 461-476.
46. Pesch M, Hülskamp M. 2004. Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation. Current Opinion in Genetics & Development 14, 422-427.
47. Pesch M, Hülskamp M. 2011. Role of TRIPTYCHON in trichome patterning in Arabidopsis. BMC Plant Biology 11, 1471-2229.
48. Reddy GV, Meyerowitz EM. 2005. Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science 310, 663-667.
49. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140.
50. Samuels AL, Glass ADM, Ehret DL, Menzies JG. 1993. The effects of silicon supplementation on cucumber fruit: changes in surface characteristics. Annals of Botany 72, 433-440.
51. Sawa S, Watanabe K, Goto K, Liu YG, Shibata D, Kanaya E, Morita EH, Okada K. 1999. FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes & Development 13, 1079-1088.
52. Schellmann S, Hülskamp M. 2005. Epidermal differentiation: trichomes in Arabidopsis as a model system. Int J Developmental Biology 49, 579-584.
53. Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, Beermann A, Thumfahrt J, Jürgens G, Hülskamp M. 2002. TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO Journal 19, 5036-5046.
54. Schwab B, Folkers U, Ilgenfritz H, Hülskamp M. 2000. Trichome morphogenesis in Arabidopsis. Philosophical Transactions of the Royal Society B: Biological Sciences 355, 879-883.
55. Serna L, Martin C. 2006. Trichomes: different regulatory networks lead to convergent structures. Trends in Plant Science 11, 274-280.
56. Simon M, Lee MM, Lin Y, Gish L, Schiefelbein J. 2007. Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Developmental Biology 311, 566-578.
57. Sinha NR, Williams RE, Hake S. 1993. Overexpression of the maize homeo box gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes & Development 7, 787-795.
58. Smith LG, Greene B, Veit B, Hake S. 1992. A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116, 21-30.
59. Szymanski DB, Jilk RA, Pollock SM, Marks MD. 1998. Control of GL2 expression in Arabidopsis leaves and trichomes. Development 125, 1161-1171.
60. Szymanski DB, Lloyd AM, Marks MD. 2000. Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis. Trends in Plant Science 5, 214-219.
61. Tian D, Tooker J, Peiffer M, Chung SH, Felton GW. 2012. Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta 236, 1053-1066.
62. Tominaga-Wada R, Nukumizu Y, Sato S, Wada T. 2013. Control of plant trichome and root-hair development by a tomato (Solanum lycopersicum) R3 MYB transcription factor. PLoS One 8, e54019.
63. Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MA, de Vries SC. 2003. The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15, 1563-1577.
64. Wada T, Kurata T, Tominaga R, Koshino-Kimura Y, Tachibana T, Goto K, Marks MD, Shimura Y, Okada K. 2002. Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129, 5409-5419.
65. Wada T, Tachibana T, Shimura Y, Okada K. 1997. Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277, 1113-1116.
66. Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Graya JC. 1999. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11, 1337-1349.
67. Wan H, Zhao Z, Qian C, Sui Y, Malik AA, Chen J. 2010. Selection of appropriate reference genes for gene expression studies by quantitative real-time polymerase chain reaction in cucumber. Analytical Biochemistry 399, 257-261.
68. Wang W, Xu B, Wang H, Li J, Huang H, Xu L. 2011. YUCCA genes are expressed in response to leaf adaxial-abaxial juxtaposition and are required for leaf margin development. Plant Physiology 157, 1805-1819.
69. Yamaguchi T, Nukazuka A, Tsukaya H. 2012. Leaf adaxial-abaxial polarity specification and lamina outgrowth: evolution and development. Plant and Cell Physiology 53, 1180-1194.
70. Yang C, Li H, Zhang J, et al. 2011. A regulatory gene induces trichome formation and embryo lethality in tomato. Proceedings of the National Academy of Sciences, USA 108, 11836-11841.
71. Zhang F, Gonzalez A, Zhao M, Payne CT, Lloyd A. 2003. A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130, 4859-4869.
72. Zhang X, Zhou Y, Ding L, Wu Z, Liu R, Meyerowitz EM. 2013. Transcription repressor HANABA TARANU controls flower development by integrating the actions of multiple hormones, floral organ specification genes, and GATA3 family genes in Arabidopsis. Plant Cell 25, 83-101.
73. Zheng Q, Wang XJ. 2008. GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Research 36, W358-W363.