Transcriptome Analysis of Cytokinin Response in Tomato Leaves

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Shi, Xiuling ^a   Gupta, Sarika ^a   Lindquist, Ingrid E ^b   Cameron, Connor T ^b   Mudge, Joann ^b   Rashotte, Aaron M ^a  

^a AUBURN UNIVERSITY   (United States)

^b NATIONAL CENTER FOR GENOME RESOURCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; CYTOKINE RECEPTOR; CYTOKININ; DIMETHYL SULFOXIDE; F BOX PROTEIN; GLUCURONOSYLTRANSFERASE; PLANT RNA; THIOREDOXIN H; UBIQUITIN CONJUGATING ENZYME E2;

ARTICLE; CONTROLLED STUDY; CYTOKININ REGULATED GENE; GENE; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC IDENTIFICATION; HORMONE RESPONSE; LEAF DEVELOPMENT; NONHUMAN; PHYTOCHEMISTRY; PLANT AGE; PLANT GENETICS; PLANT LEAF; PLANT METABOLISM; POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA SEQUENCE; RNA TRANSCRIPTION; TOMATO; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS;

CYTOKININS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE ANNOTATION; PLANT LEAVES; PRINCIPAL COMPONENT ANALYSIS; TRANSCRIPTOME;

LYCOPERSICON ESCULENTUM;

EID: 84872865623     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055090     Document Type: Article

References (93)

1. Haberer G, Kieber JJ, (2002) Cytokinins. New insights into a classic phytohormone. Plant Physiol 128: 354-362.
2. Riefler M, Novak O, Strnad M, Schmulling T, (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18: 40-54.
3. Rashotte AM, Carson SDB, To JPC, Kieber JJ, (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiol 132: 1998-2011.
4. Shani E, Ben-Gera H, Shleizer-Burko S, Burko Y, Weiss D, et al. (2010) Cytokinin regulates compound leaf development in tomato. Plant Cell 22: 3206-3217.
5. Müller B, Sheen J, (2007) Advances in cytokinin signaling. Science 318: 68-69.
6. Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, et al. (2006) A subset of Arabidopsis AP2 transcription factors mediatescytokinin responses inconcert with a two-component pathway. Proc Natl Acad Sci U S A 103: 11081-11085.
7. Shi X, Gupta S, Rashotte AM, (2012) Solanum lycopersicum cytokinin response factors (SlCRFs) genes: characterization of CRF domain containing genes in tomato. J Exp Bot 63: 973-982.
8. D'Agostino IB, Deruere J, Kieber JJ, (2000) Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol. 124: 1706-1717.
9. Brenner WG, Romanov GA, Köllmer I, Bürkle L, Schmülling T, (2005) Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. Plant J 44: 314-333.
10. Brenner WG, Ramireddy E, Heyl A, Schmülling T, (2012) Gene regulation by cytokinin in Arabidopsis. Front Plant Sci 3: 8.
11. To JP, Haberer G, Ferreira FJ, Deruere J, Mason MG, et al. (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16: 658-671.
12. Miyawaki K, Matsumoto-Kitano M, Kakimoto T, (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J. 37: 128-138.
13. Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, et al. (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci U S A 103: 16598-16603.
14. Galuszka P, PopelkováH, Werner T, Frébortová J, Pospíšilová H, et al. (2007) Biochemical characterization of cytokinin oxidases/dehydrogenases from Arabidopsis thaliana expressed in Nicotiana tabacum L. J Plant Growth Regul. 26: 255-267.
15. Hirose N, Makita N, Kojima M, Kamada-Nobusada T, Sakakibara H, (2007) Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. Plant Cell Physiol 48: 523-539.
16. Argyros RD, Mathews DE, Chiang YH, Palmer CM, Thibault DM, et al. (2008) Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20: 2102-2116.
17. Heyl A, Ramireddy E, Brenner WG, Riefler M, Allemeersch J, et al. (2008) The transcriptional repressor ARR1-SRDX suppresses pleiotropic cytokinin activities in Arabidopsis. Plant Physiol 147: 1380-1395.
18. Peleg Z, Reguera M, Tumimbang E, Walia H, Blumwald E, (2011) Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotech J 9: 747-758.
19. Rupp HM, Frank M, Werner T, Strnad M, Schmülling T, (1999) Increased steady state mRNA levels of the STM and KNAT1 homeobox genes in cytokinin overproducing Arabidopsis thaliana indicate a role for cytokinins in the shoot apical meristem. Plant J 18: 557-563.
20. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, et al. (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15: 1566-1571.
21. Alba R, Payton P, Fei Z, McQuinn R, Debbie P, et al. (2005) Transcriptome and selected fruit metabolite analysis reveal multiple points of ethylene regulatory control during tomato fruit development. Plant Cell 17: 2954-2965.
22. Rohrmann J, Tohge T, Alba R, Osorio S, Caldana C, et al. (2011) Combined transcription factor profiling, microarray analysis and metabolite profiling reveals the transcriptional control of metabolic shifts occurring during tomato fruit development. Plant J 68: 999-1013.
23. Matas AJ, Yeats TH, Buda GJ, Zheng Y, Chatterjee S, et al. (2011) Tissue- and cell type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation. Plant Cell 23: 3893-3910.
24. Schaff JE, Nielsen DM, Smith CP, Scholl EH, Bird DM, (2007) Comprehensive transcriptome profiling in tomato reveals a role for glycosyltransferase in Mi-mediated nematode resistance. Plant Physiology144: 1079-1092.
25. Cantu D, Blanco-Ulate B, Yang L, Labavitch JM, Bennett AB, et al. (2009. Ripening-regulated susceptibility of tomato fruit to Botrytis cinerea requires NOR but not RIN or ethylene. Plant Physiol 150: 1434-1449.
26. Lister R, Gregory BD, Ecker JR, (2009) Next is now: new technologies for sequencing of genomes, trancriptomes, and beyond. Curr Opin Plant Biol 12: 107-118.
27. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5: 621-628.
28. Wang Z, Gerstein M, Snyder M, (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nature Rev Genet 10: 57-63.
29. Ozsolak F, Milos PM, (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12: 87-98.
30. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
31. Robinson and Oshlack, (2010) A scaling normalization methods for differential expression analysis of RNA-seq data. Genome Biology 11: R25.
32. Taniguchi M, Kiba T, Sakakibara H, Ueguchi C, Mizuno T, et al. (1998) Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Lett 429: 259-262.
33. Mok DW, Mok MC, (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52: 89-118.
34. Schmülling T, Werner T, Riefler M, Krupkova E, Bartrina y Manns I, (2003) Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J Plant Res 116: 241-252.
35. Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, et al. (2005) Cytokinin oxidase regulates rice grain production. Science 309: 741-745.
36. Ben-Naim O, Eshed R, Parnis A, Teper-Bamnolker P, Shalit A, et al. (2006) The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA. Plant J 46: 462-476.
37. Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, et al. (2006) CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18: 2971-2984.
38. Li Y, Baldauf S, Lim EK, Bowles DJ, (2001) Phylogenetic analysis of the UDP-glycosyltransferase multigene family of Arabidopsis thaliana. J Biol Chem 276: 4338-4343.
39. Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, et al. (2010) Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. The Plant Cell 22: 2660-2679.
40. Radominska-Pandya A, Czernik PJ, Little JM, Battaglia E, Mackenzie PI, (1999) Structural and functional studies of UDP-glucuronosyltransferases. Drug Metab Rev 31: 817-899.
41. Ritter JK, (2000) Roles of glucuronidation and UDP-glucuronosyltransferases in xenobiotic bioactivation reactions. Chem Biol Interact 129: 171-193.
42. Woo HH, Faull KF, Hirsch AM, Hawes MC, (2003) Altered life cycle in Arabidopsis plants expressing PsUGT1, a UDP-glucuronosyltransferase-encoding gene from pea. Plant Physiol 133: 538-548.
43. Yendrek CR, Lee YC, Morris V, Liang Y, Pislariu CI, et al. (2010) A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula. The Plant Journal 62: 100-112.
44. Harris JM, Dickstein R, (2010) Control of root architecture and nodulation by the LATD/NIP transporter. Plant Signaling and Behavior 5: 1386-1390.
45. Golovko A, Sitbon F, Tillberg E, Nicander B, (2002) Identification of a tRNA isopentenyltransferase gene from Arabidopsis thaliana. Plant Mol. Biol. 49: 161-169.
46. Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, et al. (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci U S A 103: 16598-16603.
47. Miyawaki K, Matsumoto-Kitano M, Kakimoto T, (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37: 128-138.
48. Gray J, Gelvin SB, Meilan R, Morris RO, (1996) Transfer RNA is the source of extracellular isopentenyladenine in a Tiplasmidless strain of Agrobacterium tumefaciens. Plant Physiol 110: 431-438.
49. Koenig RL, Morris RO, Polacco JC, (2002) tRNA Is the Source of Low-Level trans-Zeatin Production in Methylobacterium spp. J Bacteriol 184: 1832-1842.
50. Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, et al. (2005) A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120: 249-259.
51. Terol J, Domingo C, Talon M, (2006) The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371: 279-290.
52. Staswick PE, Tiryaki I, (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16: 2117-2127.
53. Suza WP, Staswick PE, (2008) The role of JAR1 in jasmonoyl-Lisoleucine production in Arabidopsis wound response. Planta 227: 1221-1232.
54. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, et al. (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448: 661-665.
55. Chory J, Reinecke D, Sim S, Washburn T, Brenner M, (1994) A role for cytokinins in de-etiolation in Arabidopsis: det mutants may have an altered response to cytokinins. Plant Physiol 104: 339-347.
56. Kusnetsov VV, Herrmann RG, Kulaeva ON, Oelmüller R, (1998) Cytokinin stimulates and abscisic acid inhibits greening of etiolated Lupinus luteus cotyledons by affecting the expression of the light-sensitive protochlorophyllide oxidoreductase. Mol Gen 25: 21-28.
57. Yaronskaya R, Vershilovskaya I, Poers Y, Alawady AE, Averina N, et al. (2006) Cytokinin effects on tetrapyrrole biosynthesis and photosynthetic activity in barley seedlings. Planta 224: 700-709.
58. Okazaki K, Kabeya Y, Suzuki K, Mori T, Ichikawa T, et al. (2009) The PLASTID DIVISION1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell 21: 1769-1780.
59. Nordström A, Tarkowski P, Tarkowska D, Norbaek R, Åstot C, et al. (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana (2) a factor of potential importance for auxin-cytokinin-regulated development. Proceedings of the National Academy of Sciences, USA 101: 8039-8044.
60. Kiba T, Naitou T, Koizumi N, Yamashino T, Sakakibara H, et al. (2005) Combinatorial microarray analysis revealing Arabidopsis genes implicated in cytokinin responses through the His→Asp phosphorelay circuitry. Plant Cell Physiol. 46: 339-355.
61. Naito T, Yamashino T, Kiba T, Koizumi N, Kojima M, et al. (2007) A link between cytokinin and ASL9 (ASYMMETRIC LEAVES 2 LIKE 9) that belongs to the AS2/LOB (LATERAL ORGAN BOUNDARIES) family genes in Arabidopsis thaliana. Biosci Biotech Biochem71: 1269-1278.
62. Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H, et al. (2008) A conserved molecular framework for compound leaf development. Science 322: 1835-1839.
63. Brand A, Shirding N, Shleizer S, Ori N, (2007) Meristem maintenance andcompound-leaf patterning utilize common genetic mechanisms in tomato. Planta 226: 941-951.
64. Naito T, Yamashino T, Kiba T, Koizumi N, Kojima M, et al. (2007) A link between cytokinin and ASL9 (ASYMMETRIC LEAVES 2 LIKE 9) that belongs to the AS2/LOB (LATERAL ORGAN BOUNDARIES) family genes in Arabidopsis thaliana. Biosci Biotech Biochem 71: 1269-1278.
65. Lin WC, Shuai B, Springer PS, (2003) The Arabidopsis LATERAL ORGAN BOUNDARIES-domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial-abaxial patterning. The Plant Cell 15: 2241-2252.
66. Shuai B, Reynaga-Peña CG, Springer PS, (2002) The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiology 129: 747-761.
67. Borghi L, Bureau M, Simon R, (2007) Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. The Plant Cell 19: 1795-1808.
68. Cary AJ, Liu W, Howell SH, (1995) Cytokinin action is coupled to ethylene in its effect on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiology 107: 1075-1082.
69. Vogel JP, Woeste KE, Theologis A, Kieber JJ, (1998) Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc Natl Acad Sci U S A 95: 4766-4771.
70. Wang YP, Li L, Ye TT, Zhao SJ, Liu Z, et al. (2011) Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by down-regulating ABI5 expression. The Plant Journal 68: 249-261.
71. Weiss D, Ori N, (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiology 144: 1240-1246.
72. Wang KL, Li H, Ecker JR, (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl): S131-S151.
73. Chae HS, Faure F, Kieber JJ, (2003) The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15: 545-559.
74. Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, et al. (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 80-hydroxylases: key enzymes in ABA catabolism. EMBO J 23: 1647-1656.
75. Sakamoto T, Kobayashi M, Itoh H, Tagiri A, Kayano T, et al. (2001) Expression of a gibberellin 2-oxidase gene around the shoot apex is related to phase transition in rice. Plant Physiol 125: 1508-1516.
76. MarhavýP, Bielach A, Abas L, Abuzeineh A, Duclercq J, et al. (2011) Cytokinin modulates endocytic trafficking of pin1 auxin efflux carrier to control plant organogenesis. Dev Cell 21: 796-804.
77. Torii KU. Leucine-rich repeat receptor kinases in plants, (2004) Structure, function and signal transduction pathways. Int Rev Cytol 234: 1-46.
78. Gillissen B, Bürkle L, Andre B, Kühn C, Rentsch D, et al. (2000) A new family of high-affinity transporters for adenine, cytosine, and purine derivatives in Arabidopsis. Plant Cell 12: 291-300.
79. Bürkle L, Cedzich A, Döpke C, Stransky H, Okumoto S, et al. (2003) Transport of cytokinins mediated by purine transporters of the PUP family expressed in phloem, hydathodes, and pollen of Arabidopsis. Plant J 34: 13-26.
80. Moffatt B, Pethe C, Laloue M, (1991) Metabolism of benzyladenine is impaired in a mutant of Arabidopsis thaliana lacking adenine phosphoribosyltransferase activity. Plant Physiol 95: 900-908.
81. Allen M, Qin W, Moreau F, Moffatt B, (2002) Adenine phosphoribosyltransferase isoforms of Arabidopsis and their potential contributions to adenine and cytokinin metabolism. Physiol Plant 115: 56-68.
82. Jung KH, Seo YS, Walia H, Cao P, Fukao T, et al. (2010) The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors. Plant Physiol 152: 1674-1692.
83. Kumar R, Kushalappa K, Godt D, Pidkowich MS, Pastorelli S, et al. (2007) The Arabidopsis BEL1-LIKE HOMEODOMAIN proteins SAW1 and SAW2 act redundantly to regulate KNOX expression spatially in leaf margins. Plant Cell 19: 2719-2735.
84. Pischke MS, Huttlin EL, Hegeman AD, Sussman MR, (2006) A transcriptome-based characterization of habituation in plant tissue culture. Plant Physiol 140: 1255-1278.
85. Rashotte AM, Goertzen LR, (2010) The CRF domain defines Cytokinin Response Factor proteins in plants. BMC Plant Biol 10: 74.
86. Gordon A, Hannon GJ "FASTX-Toolkit", FASTQ/A short-reads pre-processing tools (unpublished) http://hannonlab.cshl.edu/fastx_toolkit/.
87. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, et al. (2009) ABySS: A parallel assembler for short read sequence data. Genome Res 19: 1117-1123.
88. Li R, Li Y, Kristiansen K, Wang J, (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24: 713-714.
89. Li W, Godzik A, (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
90. Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Muller WEG, et al. (2004) Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 14: 1147-1159.
91. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
92. Altschul S, Gish W, Miller W, Myers E, Lipman D, (1990) A basic local alignment search tool. J Mol Biol 215: 403-410.
93. Exposito-Rodriguez M, Borges A, Borges-Perez A, Perez J, (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol 8: 131.