Apple E3 ligase MdPUB23 mediates ubiquitin-dependent degradation of MdABI5 to delay ABA-triggered leaf senescence

Fei Yang , Ling-Ling Zhao , Lai-Qing Song , Yuepeng Han , Chun-Xiang You , Jian-Ping An

Horticulture Research ›› 2024, Vol. 11 ›› Issue (4) : 029

PDF (2233KB)
Horticulture Research ›› 2024, Vol. 11 ›› Issue (4) :029 DOI: 10.1093/hr/uhae029
Articles
research-article
Apple E3 ligase MdPUB23 mediates ubiquitin-dependent degradation of MdABI5 to delay ABA-triggered leaf senescence
Author information +
History +
PDF (2233KB)

Abstract

ABSCISIC ACID-INSENSITIVE5 (ABI5) is a core regulatory factor that mediates the ABA signaling response and leaf senescence. However, the molecular mechanism underlying the synergistic regulation of leaf senescence by ABI5 with interacting partners and the homeostasis of ABI5 in the ABA signaling response remain to be further investigated. In this study, we found that the accelerated effect of MdABI5 on leaf senescence is partly dependent on MdbHLH93, an activator of leaf senescence in apple. MdABI5 directly interacted with MdbHLH93 and improved the transcriptional activation of the senescence-associated gene MdSAG18 by MdbHLH93. MdPUB23, a U-box E3 ubiquitin ligase, physically interacted with MdABI5 and delayed ABA-triggered leaf senescence. Genetic and biochemical analyses suggest that MdPUB23 inhibited MdABI5-promoted leaf premature senescence by targeting MdABI5 for ubiquitin-dependent degradation. In conclusion, our results verify that MdABI5 accelerates leaf senescence through the MdABI5-MdbHLH93-MdSAG18 regulatory module, and MdPUB23 is responsible for the dynamic regulation of ABA-triggered leaf senescence by modulating the homeostasis of MdABI5.

Cite this article

Download citation ▾
Fei Yang, Ling-Ling Zhao, Lai-Qing Song, Yuepeng Han, Chun-Xiang You, Jian-Ping An. Apple E3 ligase MdPUB23 mediates ubiquitin-dependent degradation of MdABI5 to delay ABA-triggered leaf senescence. Horticulture Research, 2024, 11 (4) : 029 DOI:10.1093/hr/uhae029

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was financially supported by grants from the Natural Science Foundation of China (32372642), the Development Plan of the Youth Innovation Team of the Higher Education Institutions in Shandong Province (2022KJ326), and Wuhan Botanical Garden Scientific Research Support Project (E3559901).

Author contributions

J.P.A. conceived and designed the experiments. F.Y., L.L.Z., and J.P.A. performed the research. C.X.Y., L.Q.S., Y.H., and J.P.A. analyzed the data. J.P.A. wrote the paper.

Data availability

All the data generated or analyzed during this study are included in this published article. The apple gene sequences in this study can be obtained according to the following accession numbers: MdbHLH93 (MDP0000644807), MdABI5 (LOC103430245), MdPUB23 (MDP0000773851), MdSAG12 (MDP0000138228), MdSAG18 (MDP0000274609), MdNYE1 (MDP0000322543), and MdNYC1 (MDP0000124013).

Conflict of interest

The authors declare no competing interests.

References

[1]

Chinnusamy V, Gong Z, Zhu JK. Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol. 2008; 50:1187-95

[2]

Lee SC, Luan S. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ. 2012; 35:53-60

[3]

Nakashima K, Yamaguchi-Shinozaki K. ABA signaling in stress-response and seed development. Plant Cell Rep. 2013; 32:959-70

[4]

Yoshida T, Christmann A, Yamaguchi-Shinozaki K. et al. Revisiting the basal role of ABA - roles outside of stress. Trends Plant Sci. 2019; 24:625-35

[5]

Hewage KAH, Yang JF, Wang D. et al. Chemical manipulation of abscisic acid signaling: a new approach to abiotic and biotic stress management in agriculture. Adv Sci (Weinh). 2020; 7:2001265

[6]

Kavi Kishor PB, Tiozon RN Jr, Fernie AR. et al. Abscisic acid and its role in the modulation of plant growth, development, and yield stability. Trends Plant Sci. 2022; 27:1283-95

[7]

Merlot S, Gosti F, Guerrier D. et al. The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J. 2001; 25:295-303

[8]

Feng CZ, Chen Y, Wang C. et al. Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant J. 2014; 80:654-68

[9]

Ma Y, Szostkiewicz I, Korte A. et al. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science. 2009; 324:1064-8

[10]

Park SY, Fung P, Nishimura N. et al. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science. 2009; 324:1068-71

[11]

Lin Z, Li Y, Wang Y. et al. Initiation and amplification of SnRK2 activation in abscisic acid signaling. Nat Commun. 2021; 12:2456

[12]

Hasan MM, Liu XD, Waseem M. et al. ABA activated SnRK2 kinases: an emerging role in plant growth and physiology. Plant Signal Behav. 2022; 17:2071024

[13]

Raghavendra AS, Gonugunta VK, Christmann A. et al. ABA perception and signalling. Trends Plant Sci. 2010; 15:395-401

[14]

Guo J, Yang X, Weston DJ. et al. Abscisic acid receptors: past, present and future. J Integr Plant Biol. 2011; 53:469-79

[15]

Soon FF, Ng LM, Zhou XE. et al. Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science. 2012; 335:85-8

[16]

Fujii H, Chinnusamy V, Rodrigues A. et al. In vitro reconstitution of an abscisic acid signalling pathway. Nature. 2009; 462:660-4

[17]

Cutler SR, Rodriguez PL, Finkelstein RR. et al. Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol. 2010; 61:651-79

[18]

Chen K, Li GJ, Bressan RA. et al. Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol. 2020; 62:25-54

[19]

Miura K, Hasegawa PM. Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol. 2010; 20:223-32

[20]

Zhang J, Hafeez MT, Di D. et al. Precise control of ABA signaling through post-translational protein modification. Plant Growth Regul. 2019; 88:99-111

[21]

Zhang J, Hou S. Role of post-translational modification of proteins in ABA signaling transduction. Chinese Bull Bot. 2019; 54:300-15

[22]

Yang W, Zhang W, Wang X. Post-translational control of ABA signalling: the roles of protein phosphorylation and ubiquitination. Plant Biotechnol J. 2017; 15:4-14

[23]

Peng J, Schwartz D, Elias JE. et al. A proteomics approach to understanding protein ubiquitination. Nat Biotechnol. 2003; 21:921-6

[24]

Swatek KN, Komander D. Ubiquitin modifications. Cell Res. 2016; 26:399-422

[25]

Morreale FE, Walden H. Types of ubiquitin ligases. Cell. 2016; 165:248-248.e1

[26]

Trujillo M. News from the PUB: plant U-box type E3 ubiquitin ligases. J Exp Bot. 2018; 69:371-84

[27]

Zhang X, Garreton V, Chua NH. The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev. 2005; 19:1532-43

[28]

Chen YT, Liu H, Stone S. et al. ABA and the ubiquitin E3 ligase keep on going affect proteolysis of the Arabidopsis thaliana transcription factors ABF1 and ABF3. Plant J. 2013; 75:965-76

[29]

Bueso E, Rodriguez L, Lorenzo-Orts L. et al. The single-subunit RING-type E3 ubiquitin ligase RSL1 targets PYL4 and PYR1 ABA receptors in plasma membrane to modulate abscisic acid signaling. Plant J. 2014; 80:1057-71

[30]

Zhao J, Zhao L, Zhang M. et al. Arabidopsis E 3 ubiquitin ligases PUB22 and PUB23 negatively regulate drought tolerance by targeting ABA receptor PYL9 for degradation. Int J Mol Sci. 2017; 18:1841

[31]

Wu Q, Zhang X, Peirats-Llobet M. et al. Ubiquitin ligases RGLG1 and RGLG5 regulate abscisic acid signaling by controlling the turnover of phosphatase PP2CA. Plant Cell. 2016; 28:2178-96

[32]

Marino D, Froidure S, Canonne J. et al. Addendum: Arabidopsis ubiquitin ligase MIEL1 mediates degradation of the transcription factor MYB30 weakening plant defence. Nat Commun. 2019; 10:1475

[33]

Lee HG, Seo PJ. The Arabidopsis MIEL1 E3 ligase negatively regulates ABA signalling by promoting protein turnover of MYB96. Nat Commun. 2016; 7:12525

[34]

Nie K, Zhao H, Wang X. et al. The MIEL1-ABI5/MYB30 regulatory module fine tunes abscisic acid signaling during seed germination. J Integr Plant Biol. 2022; 64:930-41

[35]

Finkelstein RR, Lynch TJ. The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell. 2000; 12:599-609

[36]

Jakoby M, Weisshaar B, Dröge-Laser W. et al. bZIP transcription factors in Arabidopsis. Trends Plant Sci. 2002; 7:106-11

[37]

Skubacz A, Daszkowska-Golec A, Szarejko I. The role and regulation of ABI5 (ABA-insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Front Plant Sci. 2016; 7:1884

[38]

Bhagat PK, Verma D, Sharma D. et al. HY5 and ABI5 transcription factors physically interact to fine tune light and ABA signaling in Arabidopsis. Plant Mol Biol. 2021; 107:117-27

[39]

Song Z, Lai X, Yao Y. et al. F-box protein EBF1 and transcription factor ABI5-like regulate banana fruit chilling-induced ripening disorder. Plant Physiol. 2022; 188:1312-34

[40]

An JP, Zhang XW, Liu YJ. et al. ABI 5 regulates ABA-induced anthocyanin biosynthesis by modulating the MYB1-bHLH3 complex in apple. J Exp Bot. 2021; 72:1460-72

[41]

An JP, Zhang XW, Liu YJ. et al. MdABI5 works with its interaction partners to regulate abscisic acid-mediated leaf senescence in apple. Plant J. 2021; 105:1566-81

[42]

Liu YJ, Gao N, Ma QJ. et al. The MdABI5 transcription factor interacts with the MdNRT1.5/MdNPF7.3 promoter to fine-tune nitrate transport from roots to shoots in apple. Hortic Res. 2021; 8:236

[43]

Lyzenga WJ, Liu H, Schofield A. et al. Arabidopsis CIPK 26 interacts with KEG, components of the ABA signalling network and is degraded by the ubiquitin-proteasome system. J Exp Bot. 2013; 64:2779-91

[44]

Hu Y, Yu D. BRASSINOSTEROID INSENSITIVE 2 interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in Arabidopsis. Plant Cell. 2014; 26:4394-408

[45]

Zhou X, Hao H, Zhang Y. et al. SOS2-LIKE PROTEIN KINASE5, an SNF1-RELATED PROTEIN KINASE3-type protein KINASE, is important for abscisic acid responses in Arabidopsis through phosphorylation of ABSCISIC ACID-INSENSITIVE5. Plant Physiol. 2015; 168:659-76

[46]

Dai M, Xue Q, Mccray T. et al. The PP6 phosphatase regulates ABI5 phosphorylation and abscisic acid signaling in Arabidopsis. Plant Cell. 2013; 25:517-34

[47]

Hu R, Zhu Y, Shen G. et al. TAP46 plays a positive role in the ABSCISIC ACID INSENSITIVE5-regulated gene expression in Arabidopsis. Plant Physiol. 2014; 164:721-34

[48]

Wang XJ, Zhu SY, Lu YF. et al. Two coupled components of the mitogen-activated protein kinase cascade MdMPK1 and MdMKK 1 from apple function in ABA signal transduction. Plant Cell Physiol. 2010; 51:754-66

[49]

Miura K, Lee J, Jin JB. et al. Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci USA. 2009; 106:5418-23

[50]

Lopez-Molina L, Mongrand S, Kinoshita N. et al. AFP is a novel negative regulator of ABA signaling that promotes ABI 5 protein degradation. Genes Dev. 2003; 17:410-8

[51]

Lee JH, Yoon HJ, Terzaghi W. et al. DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E 3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell. 2010; 22:1716-32

[52]

Liu H, Stone SL. Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell. 2010; 22:2630-41

[53]

Seo KI, Lee JH, Nezames CD. et al. ABD 1 is an Arabidopsis DCAF substrate receptor for CUL4-DDB1-based E3 ligases that acts as a negative regulator of abscisic acid signaling. Plant Cell. 2014; 26:695-711

[54]

Jin D, Wu M, Li B. et al. The COP9 signalosome regulates seed germination by facilitating protein degradation of RGL2 and ABI5. PLoS Genet. 2018; 14:e1007237

[55]

Li Z, Li S, Jin D. et al. U-box E3 ubiquitin ligase PUB8 attenuates abscisic acid responses during early seedling growth. Plant Physiol. 2023; 191:2519-33

[56]

Xu X, Wan W, Jiang G. et al. Nucleocytoplasmic trafficking of the Arabidopsis WD40 repeat protein XIW1 regulates ABI5 stability and abscisic acid responses. Mol Plant. 2019; 12:1598-611

[57]

Peng J, Wang M, Wang X. et al. COP1 positively regulates ABA signaling during Arabidopsis seedling growth in darkness by mediating ABA-induced ABI5 accumulation. Plant Cell. 2022; 34:2286-308

[58]

Lim PO, Kim HJ, Nam HG. Leaf senescence. Annu Rev Plant Biol. 2007; 58:115-36

[59]

Woo HR, Kim HJ, Lim PO. et al. Leaf senescence: systems and dynamics aspects. Annu Rev Plant Biol. 2019; 70:347-76

[60]

Jibran R, Hunter DA, Dijkwel PP. Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol Biol. 2013; 82:547-61

[61]

Kim J, Kim JH, Lyu JI. et al. New insights into the regulation of leaf senescence in Arabidopsis. J Exp Bot. 2018; 69:787-99

[62]

Zhao Y, Chan Z, Gao J. et al. ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc Natl Acad Sci USA. 2016; 113:1949-54

[63]

Guo Y, Ren G, Zhang K. et al. Leaf senescence: progression, regulation, and application. Mol Hortic. 2021; 1:5

[64]

Schippers JH. Transcriptional networks in leaf senescence. Curr Opin Plant Bio. 2015; 27:77-83

[65]

Kim HJ, Nam HG, Lim PO. Regulatory network of NAC transcription factors in leaf senescence. Curr Opin Plant Biol. 2016; 33:48-56

[66]

An JP, Zhang XW, Bi SQ. et al. MdbHLH93, an apple activator regulating leaf senescence, is regulated by ABA and MdBT2 in antagonistic ways. New Phytol. 2019; 222:735-51

[67]

Wang DR, Zhang XW, Xu RR. et al. Apple U-box-type E3 ubiquitin ligase MdPUB23 reduces cold-stress tolerance by degrading the cold-stress regulatory protein MdICE1. Hortic Res. 2022; 9:uhac171

[68]

An JP, Zhang CL, Li HL. et al. Apple SINA E3 ligase MdSINA3 negatively mediates JA-triggered leaf senescence by ubiquitinating and degrading the MdBBX37 protein. Plant J. 2022; 111:457-72

[69]

Zhang XW, Xu RR, Liu Y. et al. MdVQ10 promotes wound-triggered leaf senescence in association with MdWRKY75 and undergoes antagonistic modulation of MdCML15 and MdJAZs in apple. Plant J. 2023; 115:1599-618

[70]

Asad MAU, Zakari S, Zhao Q. et al. Abiotic stresses intervene with ABA signaling to induce destructive metabolic pathways leading to death: premature leaf senescence in plants. Int J Mol Sci. 2019; 20:256

[71]

Liang C, Wang Y, Zhu Y. et al. OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proc Natl Acad Sci USA. 2014; 111:10013-8

[72]

Takasaki H, Maruyama K, Takahashi F. et al. SNAC-as, stress-responsive NAC transcription factors, mediate ABA-inducible leaf senescence. Plant J. 2015; 84:1114-23

[73]

Gao S, Gao J, Zhu X. et al. ABF2, ABF3, and ABF4 promote ABA-mediated chlorophyll degradation and leaf senescence by transcriptional activation of chlorophyll catabolic genes and senescence-associated genes in Arabidopsis. Mol Plant. 2016; 9:1272-85

[74]

Mao C, Lu S, Lv B. et al. A rice NAC transcription factor promotes leaf senescence via ABA biosynthesis. Plant Physiol. 2017; 174:1747-63

[75]

Ma X, Zhang Y, Turečková V. et al. The NAC transcription factor SlNAP2 regulates leaf senescence and fruit yield in tomato. Plant Physiol. 2018; 177:1286-302

[76]

Sakuraba Y, Jeong J, Kang MY. et al. Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat Commun. 2014; 5:4636

[77]

Chen R, Jiang H, Li L. et al. The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant Cell. 2012; 24:2898-916

[78]

Pan J, Wang H, Hu Y. et al. Arabidopsis VQ18 and VQ 26 proteins interact with ABI5 transcription factor to negatively modulate ABA response during seed germination. Plant J. 2018; 95:529-44

[79]

Hu Y, Han X, Yang M. et al. The transcription factor INDUCER OF CBF EXPRESSION1 interacts with ABSCISIC ACID INSENSITIVE5 and DELLA proteins to fine-tune abscisic acid signaling during seed germination in Arabidopsis. Plant Cell. 2019; 31:1520-38

[80]

Zhao X, Dou L, Gong Z. et al. BES1 hinders ABSCISIC ACID INSENSITIVE5 and promotes seed germination in Arabidopsis. New Phytol. 2019; 221:908-18

[81]

Guo P, Chong L, Wu F. et al. Mediator tail module subunits MED16 and MED25 differentially regulate abscisic acid signaling in Arabidopsis. J Integr Plant Biol. 2021; 63:802-15

[82]

Lopez-Molina L, Mongrand S, Chua NH. A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA. 2001; 98:4782-7

[83]

You CX, Han Y, An JP. The RGL2a-TCP46-MYB1 module regulates GA-mediated anthocyanin biosynthesis in apple. Fruit Res. 2023; 3:21

PDF (2233KB)

100

Accesses

0

Citation

Detail

Sections
Recommended

/