Abscisic acid (ABA) sensitivity regulates desiccation tolerance in germinated Arabidopsis seeds

New Phytologist

Volumn 203, Issue 1, 2014, Pages 81-93

  Maia, Julio ^a   Dekkers, Bas J W ^a,b   Dolle, Miranda J ^a   Ligterink, Wilco ^a   Hilhorst, Henk W M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

ABA signaling; ABA insensitive (abi) mutants; Abscisic acid (ABA); Arabidopsis; Desiccation tolerance (DT); Germination; Re establishment of DT; Seed development

Indexed keywords

ABSCISIC ACID; DESICCATION; DEVELOPMENTAL STAGE; DICOTYLEDON; ENVIRONMENTAL STRESS; FUNCTIONAL ROLE; GENE EXPRESSION; GERMINATION; MUTATION; OSMOSIS; SIGNALING; TOLERANCE;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ABSCISIC ACID;

ARABIDOPSIS; DESICCATION; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; OSMOTIC PRESSURE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT SEED;

ABSCISIC ACID; ARABIDOPSIS; DESICCATION; GENE EXPRESSION REGULATION, PLANT; GERMINATION; OSMOTIC PRESSURE; SEEDS; STRESS, PHYSIOLOGICAL;

EID: 84901635390     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12785     Document Type: Article

References (66)

1. Baron KN, Schroeder DF, Stasolla C. 2012. Transcriptional response of abscisic acid (ABA) metabolism and transport to cold and heat stress applied at the reproductive stage of development in Arabidopsis thaliana. Plant Science 188-189: 48-59.
2. Barros RS, Neill SJ. 1986. Periodicity of response to abscisic acid in lateral buds of willow (Salix viminalis L.). Planta 168: 530-535.
3. Bewley JD, Black M. 1994. Seeds: physiology of development and germination. New York, NY, USA: Springer.
4. Bewley JD, Bradford K, Hilhorst H, Nonogaki H. 2013. Seeds: physiology of development, germination and dormancy. New York, NY, USA: Springer.
5. Black M, Corbineau F, Gee H, Come D. 1999. Water content, raffinose, and dehydrins in the induction of desiccation tolerance in immature wheat embryos. Plant Physiology 120: 463-472.
6. Blackman SA, Obendorf RL, Leopold AC. 1992. Maturation proteins and sugars in desiccation tolerance of developing soybean seeds. Plant Physiology 100: 225-230.
7. Bruggink T, van der Toorn P. 1995. Induction of desiccation tolerance in germinated seeds. Seed Science Research 5: 1-4.
8. Buitink J, Leger JJ, Guisle I, Vu BL, Wuillème S, Lamirault G, Le Bars A, Le Meur N, Becker A, Küster H et al. 2006. Transcriptome profiling uncovers metabolic and regulatory processes occurring during the transition from desiccation-sensitive to desiccation-tolerant stages in Medicago truncatula seeds. Plant Journal 47: 735-750.
9. Buitink J, Vu BL, Satour P, Leprince O. 2003. The re-establishment of desiccation tolerance in germinated radicles of Medicago truncatula Gaertn. seeds. Seed Science Research 13: 273-286.
10. Choi H-I, Hong J-H, Ha J-O, Kang J-Y, Kim SY. 2000. ABFs, a family of ABA-responsive Element Binding Factors. Journal of Biological Chemistry 275: 1723-1730.
11. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. 2010. Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology 61: 651-679.
12. Dekkers BJW, Willems L, Bassel GW, van Bolderen-Veldkamp RP, Ligterink W, Hilhorst HWM, Bentsink L. 2012. Identification of reference genes for RT-qPCR expression analysis in Arabidopsis and tomato seeds. Plant and Cell Physiology 53: 28-37.
13. Finkelstein R, Gampala SSL, Lynch TJ, Thomas TL, Rock CD. 2005. Redundant and distinct functions of the ABA response loci ABA-insensitive (ABI)5 and ABRE-binding factor (ABF)3. Plant Molecular Biology 59: 253-267.
14. Finkelstein RR. 1994. Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant Journal 5: 765-771.
15. Finkelstein RR, Li Wang M, Lynch TJ, Rao S, Goodman HM. 1998. The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA2 domain protein. Plant Cell 10: 1043-1054.
16. Finkelstein RR, Lynch TJ. 2000a. Abscisic acid inhibition of radicle emergence but not seedling growth is suppressed by sugars. Plant Physiology 122: 1179-1186.
17. Finkelstein RR, Lynch TJ. 2000b. The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12: 599-609.
18. Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North HM, Marion-Poll A. 2012. Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. Plant Journal 70: 501-512.
19. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K. 2011. ABA-mediated transcriptional regulation in response to osmotic stress in plants. Journal of Plant Research 124: 509-525.
20. Furtado DF. 2011. Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia 35: 1039-1042.
21. Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM. 1992. Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4: 1251-1261.
22. Gosti F, Beaudoin N, Serizet C, Webb AAR, Vartanian N, Giraudat J. 1999. ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11: 1897-1909.
23. Gutierrez L, Van Wuytswinkel O, Castelain M, Bellini C. 2007. Combined networks regulating seed maturation. Trends in Plant Science 12: 294-300.
24. Illing N, Denby KJ, Collett H, Shen A, Farrant JM. 2005. The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integrative and Comparative Biology 45: 771-787.
25. Ishitani M, Xiong L, Stevenson B, Zhu JK. 1997. Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9: 1935-1949.
26. Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F. 2002. bZIP transcription factors in Arabidopsis. Trends in Plant Science 7: 106-111.
27. Jia H, Suzuki M, McCarty DR. 2013. Regulation of the seed to seedling developmental phase transition by the LAFL and VAL transcription factor networks. Wiley Interdisciplinary Reviews: Developmental Biology 3: 135-145.
28. Kim SY, Chung H-J, Thomas TL. 1997. Isolation of a novel class of bZIP transcription factors that interact with ABA-responsive and embryo-specification elements in the Dc3 promoter using a modified yeast one-hybrid system. Plant Journal 11: 1237-1251.
29. Koornneef M, Reuling G, Karssen C. 1984. The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiologia Plantarum 61: 377-383.
30. Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ. 2006. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126: 1109-1120.
31. Léon-Kloosterziel KM, Gil MA, Ruijs GJ, Jacobsen SE, Olszewski NE, Schwartz SH, Zeevaart JAD, Koornneef M. 1996. Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant Journal 10: 655-661.
32. Leopold AC, Vertucci CW. 1986. Membranes, metabolism and dry organisms. In: Leopold AC, ed. Physical attributes of desiccated seeds. London, UK: Comstock Publishing, 23-34.
33. Leung J, Merlot S, Giraudat J. 1997. The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9: 759-771.
34. Lopez-Molina L, Chua N-H. 2000. A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana. Plant and Cell Physiology 41: 541-547.
35. Lopez-Molina L, Mongrand S, Chua N-H. 2001. A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proceedings of the National Academy of Sciences, USA 98: 4782-4787.
36. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064-1068.
37. Maia J, Dekkers BJW, Provart NJ, Ligterink W, Hilhorst HWM. 2011. The re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds and its associated transcriptome. PLoS ONE 6: e29123.
38. Miyakawa T, Fujita Y, Yamaguchi-Shinozaki K, Tanokura M. 2013. Structure and function of abscisic acid receptors. Trends in Plant Science 18: 259-266.
39. Nambara E, Marion-Poll A. 2005. Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology 56: 165-185.
40. Nambara E, Naito S, McCourt P. 1992. A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele. Plant Journal 2: 435-441.
41. Nambara E, Suzuki M, Abranis S, McCartjy DR, Kaniiya Y, McCourt P. 2002. A screen for genes that function in abscisic acid signaling in Arabidopsis thaliana. Genetics 161: 1247-1255.
42. Nedeva D, Nikolova A. 1997. Desiccation tolerance in developing seeds. Bulgarian Journal of Plant Physiology 23: 100-113.
43. Ooms JJJ, Léon-Kloosterziel KM, Bartels D, Koornneef M, Karssen CM. 1993. Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana: a comparative study using abscisic acid-insensitive abi3 mutants. Plant Physiology 102: 1185-1191.
44. Ooms JJJ, Veen R, Karssen CM. 1994. Abscisic acid and osmotic stress or slow drying independently induce desiccation tolerance in mutant seeds of Arabidopsis thaliana. Physiologia Plantarum 92: 506-510.
45. Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-fF et al. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071.
46. Priest DM, Ambrose SJ, Vaistij FE, Elias L, Higgins GS, Ross ARS, Abrams SR, Bowles DJ. 2006. Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant Journal 46: 492-502.
47. Raghavendra AS, Gonugunta VK, Christmann A, Grill E. 2010. ABA perception and signaling. Trends in Plant Science 15: 395-401.
48. Ramakers C, Ruijter JM, Lekanne Deprez RH, Moorman AFM. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339: 62-66.
49. Saika H, Okamoto M, Miyoshi K, Kushiro T, Shinoda S, Jikumaru Y, Fujimoto M, Arikawa T, Takahashi H, Ando M et al. 2007. Ethylene promotes submergence-induced expression of OsABA8ox1, a gene that encodes ABA 8′-hydroxylase in rice. Plant and Cell Physiology 48: 287-298.
50. Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L. 2008. Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant Journal 54: 608-620.
51. Sreedhar L. 2002. In vivo characterization of the effects of abscisic acid and drying protocols associated with the acquisition of desiccation tolerance in alfalfa (Medicago sativa L.) somatic embryos. Annals of Botany 89: 391-400.
52. To A, Valon C, Savino G, Guilleminot J, Devic M, Giraudat J, Parcy F. 2006. A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18: 1642-1651.
53. Toufighi K, Brady SM, Austin R, Ly E, Provart NJ. 2005. The botany array resource: e-Northerns, expression angling, and promoter analyses. Plant Journal 43: 153-163.
54. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K. 2010. Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiology 51: 1821-1839.
55. Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K. 2009. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proceedings of the National Academy of Sciences, USA 106: 17588-17593.
56. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K. 2000. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proceedings of the National Academy of Sciences, USA 97: 11632-11637.
57. Van Leeuwen W, Hagendoorn MJM, Ruttink T, Van Poecke R, Van Der Plas LHW, Van Der Krol AR. 2000. The use of the luciferase reporter system for in planta gene expression studies. Plant Molecular Biology Reporter 18: 143a-143t.
58. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: RESEARCH0034.
59. Verdier J, Lalanne D, Pelletier S, Torres-Jerez I, Righetti K, Bandyopadhyay K, Leprince O, Chatelain E, Ly Vu B, Gouzy J et al. 2013. A regulatory network-based approach dissects late maturation processes related to the acquisition of desiccation tolerance and longevity of Medicago truncatula seeds. Plant Physiology 163: 757-774.
60. Vieira CV, Amaral da Silva E, Alvarenga AA, de Castro EM, Toorop PE. 2010. Stress-associated factors increase after desiccation of germinated seeds of Tabebuia impetiginosa Mart. Plant Growth Regulation 62: 257-263.
61. Wan CY, Wilkins TA. 1994. A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Analytical Biochemistry 223: 7-12.
62. Westwood JH, McCann L, Naish M, Dixon H, Murphy AM, Stancombe MA, Bennett MH, Powell G, Webb AAR, Carr JP. 2013. A viral RNA silencing suppressor interferes with abscisic acid-mediated signaling and induces drought tolerance in Arabidopsis thaliana. Molecular Plant Pathology 14: 158-170.
63. Xu N, Bewley JD. 1995. The role of abscisic acid in germination, storage protein synthesis and desiccation tolerance in alfalfa (Medicago sativa L.) seeds, as shown by inhibition of its synthesis by fluridone during development. Journal of Experimental Botany 46: 687-694.
64. Yamaguchi-Shinozaki K, Shinozaki K. 1993. Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Molecular and General Genetics 236: 331-340.
65. Yamaguchi-Shinozaki K, Shinozaki K. 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57: 781-803.
66. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2010. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant Journal 61: 672-685.