Diurnal oscillations of soybean circadian clock and drought responsive genes

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Marcolino Gomes, Juliana ^a,b   Rodrigues, Fabiana Aparecida ^a   Fuganti Pagliarini, Renata ^a   Bendix, Claire ^c,d   Nakayama, Thiago Jonas ^e   Celaya, Brandon ^c,d   Molinari, Hugo Bruno Correa ^f   De Oliveira, Maria Cristina Neves ^a   Harmon, Frank G ^c,d   Nepomuceno, Alexandre ^a,f  

^a EMBRAPA CERRADOS   (Brazil)

^b STATE UNIVERSITY OF LONDRINA   (Brazil)

^c WESTERN REGIONAL RESEARCH CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^f PLANT GENE EXPRESSION CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID;

ARTICLE; BZIP GENE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DREB GENE; DROUGHT; ELF4 GENE; GENE EXPRESSION; GOLS GENE; LCL1 GENE; LUX GENE; NONHUMAN; PLANT GENE; PLANT STRESS; PROMOTER REGION; PRR GENE; PRR7 GENE; RAB18 GENE; REMORIN GENE; SOYBEAN; TOC1 GENE;

ABSCISIC ACID; ADAPTATION, PHYSIOLOGICAL; ANALYSIS OF VARIANCE; ARABIDOPSIS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, RNA; SOYBEANS;

EID: 84899950884     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086402     Document Type: Article

References (80)

1. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. Journal of experimental botany 58: 221-227. (Pubitemid 46204209)
2. Melcher K, Ng L-M, Zhou XE, Soon F-F, Xu Y, et al. (2009) A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462: 602-608.
3. Wu F-Q, Xin Q, Cao Z, Liu Z-Q, Du S-Y, et al. (2009) The magnesiumchelatase H subunit binds abscisic acid and functions in abscisic acid signaling: new evidence in Arabidopsis. Plant physiology 150: 1940-1954.
4. Weltmeier F, Rahmani F, Ehlert A, Dietrich K, Schütze K, et al. (2009) Expression patterns within the Arabidopsis C/S1 bZIP transcription factor network: availability of heterodimerization partners controls gene expression during stress response and development. Plant molecular biology 69: 107-119.
5. Zhang G, Chen M, Li L, Xu Z, Chen X, et al. (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. Journal of experimental botany 60: 3781-3796.
6. Santos TB, Budzinski IGF, Marur CJ, Petkowicz CLO, Pereira LFP, et al. (2011) Expression of three galactinol synthase isoforms in Coffea arabica L. and accumulation of raffinose and stachyose in response to abiotic stresses. Plant physiology and biochemistry: PPB/Société française de physiologie végétale 49: 441-448.
7. Agarwal P, Reddy MK, Sopory SK, Agarwal PK (2009) Plant Rabs: Characterization, Functional Diversity, and Role in Stress Tolerance. Plant Molecular Biology Reporter 27: 417-430.
8. Raffaele S, Mongrand S, Gamas P, Niebel A, Ott T (2007) Genome-wide annotation of remorins, a plant-specific protein family: evolutionary and functional perspectives. Plant physiology 145: 593-600. (Pubitemid 350127592)
9. Khanna-Chopra R, Selote DS (2007) Acclimation to drought stress generates oxidative stress tolerance in drought-resistant than -susceptible wheat cultivar under field conditions. Environmental and Experimental Botany 60: 276-283. (Pubitemid 46367873)
10. Legnaioli T, Cuevas J, Mas P (2009) TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. The EMBO journal 28: 3745-3757.
11. Wilkins O, Bräutigam K, Campbell MM (2010) Time of day shapes Arabidopsis drought transcriptomes. The Plant journal: for cell and molecular biology 63: 715-727.
12. Pokhilko A, Fernández AP, Edwards KD, Southern MM, Halliday KJ, et al. (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Molecular systems biology 8: 574.
13. Harmer SL (2000) Orchestrated Transcription of Key Pathways in Arabidopsis by the Circadian Clock. Science 290: 2110-2113.
14. Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, et al. (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science (New York, NY) 293: 880-883. (Pubitemid 32743980)
15. Gendron JM, Pruneda-Paz JL, Doherty CJ, Gross AM, Kang SE, et al. (2012) Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proceedings of the National Academy of Sciences of the United States of America 109: 3167-3172.
16. Dixon LE, Knox K, Kozma-Bognar L, Southern MM, Pokhilko A, et al. (2011) Temporal repression of core circadian genes is mediated through EARLY FLOWERING 3 in Arabidopsis. Current biology: CB 21: 120-125.
17. Helfer A, Nusinow DA, Chow BY, Gehrke AR, Bulyk ML, et al. (2011) LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Current biology: CB 21: 126-133.
18. Kikis EA, Khanna R, Quail PH (2005) ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. The Plant journal: for cell and molecular biology 44: 300-313.
19. Farré EM, Harmer SL, Harmon FG, Yanovsky MJ, Kay SA (2005) Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Current biology: CB 15: 47-54.
20. Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua N-H, et al. (2010) PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. The Plant cell 22: 594-605.
21. Kim W-Y, Fujiwara S, Suh S-S, Kim J, Kim Y, et al. (2007) ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449: 356-360. (Pubitemid 47443478)
22. Song YH, Ito S, Imaizumi T (2010) Similarities in the circadian clock and photoperiodism in plants. Current opinion in plant biology 13: 594-603.
23. Liu H, Wang H, Gao P, Xü J, Xü T, et al. (2009) Analysis of clock gene homologs using unifoliolates as target organs in soybean (Glycine max). Journal of plant physiology 166: 278-289.
24. Sullivan S, Jenkins G, Nimmo H (2004) Roots, cycles and leaves. Expression of the phosphoenolpyruvate carboxylase kinase gene family in soybean. Plant physiology 135: 2078-2087. (Pubitemid 39182787)
25. Hudson KA (2010) The Circadian Clock-controlled Transcriptome of Developing Soybean Seeds. The Plant Genome Journal 3: 3.
26. Thakare D, Kumudini S, Dinkins RD (2010) Expression of flowering-time genes in soybean E1 near-isogenic lines under short and long day conditions. Planta 231: 951-963.
27. Bieniawska Z, Espinoza C, Schlereth A, Sulpice R, Hincha DK, et al. (2008) Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant physiology 147: 263-279. (Pubitemid 352844361)
28. Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant physiology 137: 961-968. (Pubitemid 43138168)
29. Sanchez A, Shin J, Davis SJ (2011) Abiotic stress and the plant circadian clock. Plant Signaling & Behavior 6: 223-231.
30. Oya T, Nepomuceno AL, Neumaier N, Renato J, Farias B, et al. (2004) Drought Tolerance Characteristics of Brazilian Soybean Cultivars: Evaluation and characterization of drought tolerance of various Brazilian soybean cultivars in the field. Plant Production Science 7: 129-137. (Pubitemid 38818947)
31. Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of Development Descriptions for Soybeans, Glycine Max (L.) Merrill1. Crop Science 11: 929.
32. Jian B, Liu B, Bi Y, Hou W, Wu C, et al. (2008) Validation of internal control for gene expression study in soybean by quantitative real-time PCR. BMC molecular biology 9: 59.
33. Stolf-Moreira R, Lemos EG de M, Abdelnoor RV, Beneventi MA, Rolla AAP, et al. (2011) Identification of reference genes for expression analysis by real-time quantitative PCR in drought-stressed soybean. Pesquisa agropecuaria brasileira 46: 58-65.
34. Rodrigues FA, Marcolino-Gomes J, Carvalho JFC, do Nascimento LC, Neumaier N, et al. (2012) Subtractive libraries for prospecting differentially expressed genes in the soybean under water deficit. Genetics and molecular biology 35: 304-314.
35. Mizuno T, Yamashino T (2008) Comparative transcriptome of diurnally oscillating genes and hormone-responsive genes in Arabidopsis thaliana: insight into circadian clock-controlled daily responses to common ambient stresses in plants. Plant & cell physiology 49: 481-487. (Pubitemid 351398304)
36. Yuan JS, Reed A, Chen F, Stewart CN (2006) Statistical analysis of real-time PCR data. BMC bioinformatics 7: 85.
37. Porter S, Olson NE, Smith T (2009) Analyzing gene expression data from microarray and next-generation dna sequencing transcriptome profiling assays using GeneSifter analysis edition.
38. Altschul SF, Gish W, Pennsylvania T, Park U (1990) Basic Local Alignment Search Tool. Journal of molecular biology 215: 403-410.
39. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular biology and evolution 4: 406-425.
40. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular biology and evolution 28: 2731-2739.
41. Felsenstein J (1985) Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution 39: 783-791.
42. Tomii K, Sawada Y, Honda S (2012) Convergent evolution in structural elements of proteins investigated using cross profile analysis. BMC bioinformatics 13: 11.
43. Marsh HW (1998) Pairwise deletion for missing data in structural equation models: Nonpositive definite matrices, parameter estimates, goodness of fit, and adjusted sample sizes. Structural Equation Modeling 5: 22-36.
44. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, et al. (2005) MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics (Oxford, England) 21: 2933-2942. (Pubitemid 40916416)
45. Quandt K, Frech K, Karas H, Wingender E, Werner T (1995) MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic acids research 23: 4878-4884. (Pubitemid 3008389)
46. Severin AJ, Cannon SB, Graham MM, Grant D, Shoemaker RC (2011) Changes in twelve homoeologous genomic regions in soybean following three rounds of polyploidy. The Plant cell 23: 3129-3136.
47. Jänkänpää HJ, Mishra Y, Schröder WP, Jansson S (2012) Metabolic profiling reveals metabolic shifts in Arabidopsis plants grown under different light conditions. Plant, cell & environment 35: 1824-1836.
48. Thines B, Harmon FG (2010) Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock. Proceedings of the National Academy of Sciences of the United States of America 107: 3257-3262.
49. Baerenfaller K, Massonnet C, Walsh S, Baginsky S, Bühlmann P, et al. (2012) Systems-based analysis of Arabidopsis leaf growth reveals adaptation to water deficit. Molecular systems biology 8: 606.
50. Jiang Y, Han YZ, Zhang XM (2011) Expression profiles of a CONSTANS homologue GmCOL11 in Glycine max. Russian Journal of Plant Physiology 58: 928-935.
51. Lu SX, Knowles SM, Webb CJ, Celaya RB, Cha C, et al. (2011) The Jumonji C domain-containing protein JMJ30 regulates period length in the Arabidopsis circadian clock. Plant physiology 155: 906-915.
52. Huang W, Pérez-Garcia P, Pokhilko A, Millar AJ, Antoshechkin I, et al. (2012) Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science (New York, NY) 336: 75-79.
53. Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, et al. (2002) LHY and CCA1 Are Partially Redundant Genes Required to Maintain Circadian Rhythms in Arabidopsis. Developmental Cell 2: 629-641. (Pubitemid 34538143)
54. Hazen SP, Schultz TF, Pruneda-Paz JL, Borevitz JO, Ecker JR, et al. (2005) LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proceedings of the National Academy of Sciences of the United States of America 102: 10387-10392. (Pubitemid 41023380)
55. McWatters HG, Kolmos E, Hall A, Doyle MR, Amasino RM, et al. (2007) ELF4 is required for oscillatory properties of the circadian clock. Plant physiology 144: 391-401. (Pubitemid 46941642)
56. Li G, Siddiqui H, Teng Y, Lin R, Wan X, et al. (2011) Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis. Nature cell biology 13: 616-622.
57. Ibáñez C, Kozarewa I, Johansson M, Ogren E, Rohde A, et al. (2010) Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. Plant physiology 153: 1823-1833.
58. Ramos A, Pérez-Solís E, Ibáñez C, Casado R, Collada C, et al. (2005) Winter disruption of the circadian clock in chestnut. Proceedings of the National Academy of Sciences of the United States of America 102: 7037-7042. (Pubitemid 40675436)
59. Dong MA, Farré EM, Thomashow MF (2011) Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 108: 7241-7246.
60. Govind G, Harshavardhan VT, ThammeGowda HV, Patricia JK, Kalaiarasi PJ, et al. (2009) Identification and functional validation of a unique set of drought induced genes preferentially expressed in response to gradual water stress in peanut. Molecular genetics and genomics: MGG 281: 591-605.
61. Chen Z, Zang J, Whetstine J, Hong X, Davrazou F, et al. (2006) Structural insights into histone demethylation by JMJD2 family members. Cell 125: 691-702.
62. Jones MA, Covington MF, DiTacchio L, Vollmers C, Panda S, et al. (2010) Jumonji domain protein JMJD5 functions in both the plant and human circadian systems. Proceedings of the National Academy of Sciences of the United States of America 107: 21623-21628.
63. Boyko A, Kathiria P, Zemp FJ, Yao Y, Pogribny I, et al. (2007) Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (virus-induced plant genome instability). Nucleic acids research 35: 1714-1725. (Pubitemid 46592888)
64. Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environmental and molecular mutagenesis 49: 61-72. (Pubitemid 351293012)
65. Choi C-S, Sano H (2007) Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Molecular genetics and genomics: MGG 277: 589-600. (Pubitemid 46644070)
66. Wang M, Yu D, Guo X, Cui Y, Li X, et al. (2011) Casein kinase 1-Like 3 is required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. African Journal of Biotechnology 10: 13219-13229. doi:10.5897/AJB11.2086.
67. Preuss SB, Meister R, Xu Q, Urwin CP, Tripodi FA, et al. (2012) Expression of the Arabidopsis thaliana BBX32 gene in soybean increases grain yield. PloS one 7: e30717.
68. Mikkelsen MD, Thomashow MF (2009) A role for circadian evening elements in cold-regulated gene expression in Arabidopsis. The Plant journal: for cell and molecular biology 60: 328-339.
69. Robertson FC, Skeffington AW, Gardner MJ, Webb AA (2009) Interactions between circadian and hormonal signalling in plants. Plant molecular biology 69: 419-427.
70. Marcolino-Gomes J, Rodrigues FA, Oliveira MCN, Farias JRB, Neumaier N, et al. (2013) Expression Patterns of GmAP2/EREB-Like Transcription Factors Involved in Soybean Responses to Water Deficit. PloS one 8: e62294.
71. Maruyama K, Todaka D, Mizoi J, Yoshida T, Kidokoro S, et al. (2012) Identification of cis-acting promoter elements in cold- and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA research: an international journal for rapid publication of reports on genes and genomes 19: 37-49.
72. Gao S-Q, Chen M, Xu Z-S, Zhao C-P, Li L, et al. (2011) The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant molecular biology 75: 537-553.
73. Müller AH, Hansson M (2009) The barley magnesium chelatase 150-kd subunit is not an abscisic acid receptor. Plant physiology 150: 157-166.
74. Boneh U, Biton I, Schwartz A, Ben-Ari G (2012) Characterization of the ABA signal transduction pathway in Vitis vinifera. Plant science: an international journal of experimental plant biology 187: 89-96.
75. Liu B, Fan J, Zhang Y, Mu P, Wang P, et al. (2012) OsPFA-DSP1, a rice protein tyrosine phosphatase, negatively regulates drought stress responses in transgenic tobacco and rice plants. Plant cell reports 31: 1021-1032.
76. Pruneda-Paz JL, Breton G, Para A, Kay SA (2009) A Functional Genomics Approach Reveals CHE as a Component of the Arabidopsis Circadian Clock. Nature 323: 1481-1486.
77. Rushton DL, Tripathi P, Rabara RC, Lin J, Ringler P, et al. (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant biotechnology journal 10: 2-11.
78. Ying S, Zhang D-F, Fu J, Shi Y-S, Song Y-C, et al. (2012) Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis. Planta 235: 253-266.
79. Rugnone ML, Faigón Soverna A, Sanchez SE, Schlaen RG, Hernando CE, et al. (2013) LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator. Proceedings of the National Academy of Sciences of the United States of America 110: 12120-12125.
80. Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annual review of plant biology 53: 247-273.