Functional Involvement of Highly Abscisic Acid-Induced Clade A Protein Phosphatase 2Cs in Delayed Seed Germination Under Cold Stress

다국어 초록 (Multilingual Abstract)

Seed germination represents a vital stage in the life cycle of plants, in which the phytohormone abscisic acid (ABA) plays important modulatory roles, including the promotion of seed dormancy and inhibition of germination. The Arabidopsis genome contains nine clade A protein phosphatases (PP2Cs), which in conjunction with PYR1/PYLs/RCARs, function as ABA co-receptors. However, the precise role of these PP2Cs in seeds is yet to be ascertained. In this study, we report the functional involvement of HIGHLY ABA-INDUCED (HAI) PP2Cs, including AIP1/HAI2, HAI1, and HAI3, in cold stress-induced inhibition of germination. The expression of HAI PP2C genes in dry seeds was found to be dependent on ABA, and the expression levels decreased as the seeds germinated. Under cold stress conditions, germination of the seeds of HAI PP2C knockout mutants was observed to be significantly slower than that of wild-type seeds, with the aip1-1 mutant showing a notably stronger inhibition of germination than other PP2C mutants. This distinct phenotype of aip1-1 was determined at the pre-germinative stage and demonstrated to be compromised by the inhibition of ABA synthesis. Our data indicate that AIP1 could be the main PP2C involved in ABA-mediated inhibition of germination under cold stress conditions. We speculate that this protein functions downstream of RCAR5/PYL11 and contributes to the regulation of seed germination by interacting with RCAR5/PYL11 in the presence of ABA.

참고문헌 (Reference)

1 Bhaskara GB, "Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs" 160 : 379-395, 2012

2 Umezawa T, "Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis" 106 : 17588-17593, 2009

3 Shu K, "Two faces of one seed : hormonal regulation of dormancy and germination" 9 : 34-45, 2016

4 Rubio S, "Triple loss of function of protein phosphatases type 2C leads to partial constitutive response to endogenous abscisic acid" 150 : 1345-1355, 2009

5 Sato A, "Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2. 6 protein kinase" 424 : 439-448, 2009

6 Fujita Y, "Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis" 50 : 2123-2132, 2009

7 Koornneef M, "The isolation of abscisic-acid(Aba)defcient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana(L)Heynh" 61 : 385-393, 1982

8 Koornneef M, "The isolation and characterization of abscisic-acid insensitive mutants of Arabidopsis thaliana" 61 : 377-383, 1984

9 Kushiro T, "The Arabidopsis cytochrome P450CYP707A encodes ABA 8’-hydroxylases : key enzymes in ABA catabolism" 23 : 1647-1656, 2004

10 Merlot S, "The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway" 25 : 295-303, 2001

11 Benvenuti S, "Soil physics involvement in the germination ecology of buried weed seeds" 8 : 7-, 2019

12 Antoni R, "Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors" 158 : 970-980, 2012

13 Bentsink L, "Seed dormancy and germination" 6 : e0119-, 2008

14 Millar AA, "Seed dormancy and ABA metabolism in Arabidopsis and barley : the role of ABA 8’-hydroxylase" 45 : 942-954, 2006

15 Nonogaki H, "Seed biology updates—highlights and new discoveries in seed dormancy and germination research" 8 : 524-, 2017

16 Kermode AR, "Role of abscisic acid in seed dormancy" 24 : 319-344, 2005

17 Ma Y, "Regulators of PP2C phosphatase activity function as abscisic acid sensors" 324 : 1064-1068, 2009

18 Seo M, "Regulation of hormone metabolism in Arabidopsis seeds : phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism" 48 : 354-366, 2006

19 Bakhshandeh E, "Quantifcation of the efect of environmental factors on seed germination and seedling growth of Eruca(Eruca sativa)using mathematical models" 39 : 190-204, 2020

20 Miransari M, "Plant hormones and seed germination" 99 : 110-121, 2014

21 Kucera B, "Plant hormone interactions during seed dormancy release and germination" 15 : 281-307, 2005

22 Schweighofer A, "Plant PP2C phosphatases : emerging functions in stress signaling" 9 : 236-243, 2004

23 Hirayama T, "Perception and transduction of abscisic acid signals : keys to the function of the versatile plant hormone ABA" 12 : 343-351, 2007

24 Guo XH, "Mutational analysis of Arabidopsis PP2CA2 involved in abscisic acid signal transduction" 37 : 763-769, 2010

25 Soon FF, "Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases" 335 : 85-88, 2012

26 Finkelstein R, "Molecular aspects of seed dormancy" 59 : 387-415, 2008

27 Finkelstein RR, "Maternal efects govern variable dominance of 2 abscisic-acid response mutations in Arabidopsis thaliana" 105 : 1203-1208, 1994

28 Nishimura N, "Isolation and characterization of novel mutants afecting the abscisic acid sensitivity of Arabidopsis germination and seedling growth" 45 : 1485-1499, 2004

29 Xue TT, "Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis" 9 : 550-, 2008

30 Ludwikow A, "Gene expression profling of ozone-treated Arabidopsis abi1td insertional mutant : protein phosphatase 2C ABI1 modulates biosynthesis ratio of ABA and ethylene" 230 : 1003-1017, 2009

31 Saez A, "Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1reveal its role as a negative regulator of abscisic acid signalling" 37 : 354-369, 2004

32 Lim CW, "Functional roles of the protein phosphatase 2C, AtAIP1, in abscisic acid signaling and sugar tolerance in Arabidopsis" 187 : 83-88, 2012

33 Yoshida T, "Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress" 38 : 35-49, 2015

34 El-Keblawy A, "Efect of maturation conditions on light and temperature requirements during seed germination of Citrullus colocynthis from the Arabian Desert" 21 : 292-299, 2019

35 Nishimura N, "Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme" 9 : 1-14, 2018

36 Mbarki S, "Comparing salt tolerance at seedling and germination stages in local populations of Medicago ciliaris L. to Medicago intertexta L. and Medicago scutellata L" 9 : 526-, 2020

37 Niyogi KK, "Arabidopsis mutants defne a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion" 10 : 1121-1134, 1998

38 Livak KJ, "Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C)method" 25 : 402-408, 2001

39 Merai Z, "Aethionema arabicum : a novel model plant to study the light control of seed germination" 70 : 3313-3328, 2019

40 Geiger D, "Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair" 106 : 21425-21430, 2009

41 Park SY, "Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins" 324 : 1068-1071, 2009

42 Cutler SR, "Abscisic acid : emergence of a core signaling network" 61 (61): 651-679, 2010

43 Yoshida T, "ABA-hypersensitive germination3 encodes a protein phosphatase 2C(AtPP2CA)that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs" 140 : 115-126, 2006

44 Lim CW, "ABA-dependent and ABA-independent functions of RCAR5/PYL11 in response to cold stress" 11 : 587620-, 2020

45 Nishimura N, "ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed" 50 : 935-949, 2007

46 Lee SC, "A protein kinasephosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells" 106 : 21419-21424, 2009

47 Lim CW, "A prominent role for RCAR3-mediated ABA signaling in response to Pseudomonas syringae pv. tomato DC3000 infection in Arabidopsis" 55 : 1691-1703, 2014