Skip to main content
SpringerLink
Log in

Arabidopsis ABSCISIC ACID INSENSITIVE4 targets PROTEIN L-ISOASPARTYL METHYLTRANSFERASE1 in seed

  • Short Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Arabidopsis ABSCISIC ACID INSENSITIVE4 (ABI4) positively regulates the protein repairing enzyme (PRE) PROTEIN L-ISOASPARTYL METHYLTRANSFERASE1 (PIMT1) in seed for its implication in seed vigor and longevity.

Abstract

PROTEIN L-ISOASPARTYL METHYLTRANSFERASE (PIMT) is a protein repairing enzyme (PRE) and is implicated in seed vigor and longevity. PIMT has been shown to be induced by ABA, however, its detailed regulation by ABA signaling components is unknown. Herein, we report that ABSCISIC ACID INSENSITIVE4 (ABI4) directly binds to the PIMT1 promoter and regulates its expression in Arabidopsis seeds. AtPIMT1 promoter analysis demonstrated the presence of putative ABI4 binding sites. Our Y1H analysis revealed that AtABI4 transcription factor binds to the AtPIMT1 promoter. Dual luciferase assay also demonstrated the binding of the AtABI4 transcription factor to the AtPIMT1 promoter. Subsequently, we have generated AtPIMT1 promoter GUS lines and revealed that ABA induced expression of GUS in Arabidopsis thaliana. Expression analyses exhibited reduced accumulation of PIMT1 protein and transcript with significant reduction in total PIMT activity in abi4-1 mutants as compared to that of the wild type. The AtPIMT1 promoter GUS expression in abi4-1 mutants was also found to be severely affected in both the control and ABA treatment. Hence, through molecular and genetic evidences we show that the AtABI4 plays a central role in regulating the expression of AtPIMT1 to impart seed vigor and longevity to orthodox seeds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Data availability statement

Sequence information of this article can be found in The Arabidopsis Information Resource (www.arabidopsis.org) under the following accession numbers: AtPIMT1 (At3g48330); AtABI4 (At2g40220); AtABI5 (At2g36270); AtUBQ10 (At4g05320).

Abbreviations

ABI:

Abscisic acid insensitive

isoAsp:

Isoaspartate

PIMT:

Protein l-isoaspartyl methyltransferase

PRE:

Protein repairing enzyme

References

  • Bossi F, Cordoba E, Dupré P, Mendoza MS, Román CS, León P (2009) The Arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2.2 genes during sugar signalling. Plant J 59:359–374

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Ghosh S, Kamble NU, Verma P, Salvi P, Petla BP, Roy S, Rao V, Hazra A, Varshney V, Kaur H, Majee M (2020a) Arabidopsis protein L-ISOASPARTYL METHYLTRANSFERASE repairs isoaspartyl damage to antioxidant enzymes and increases heat and oxidative stress tolerance. J Biol Chem 295:783–799

    Article  Google Scholar 

  • Ghosh S, Kamble NU, Majee M (2020b) A protein repairing enzyme, PROTEIN L-ISOASPARTYL METHYLTRANSFERASE is involved in salinity stress tolerance by increasing efficiency of ROS-scavenging enzymes. Environ Exp Bot 180:104266

    Article  CAS  Google Scholar 

  • Johnson BA, Langmack EL, Aswad DW (1987) Partial repair of deamidation-damaged calmodulin by protein carboxyl methyltransferase. J Biol Chem 262:12283–12287

    Article  CAS  Google Scholar 

  • Kamble NU, Majee M (2022) PROTEIN L-ISOASPARTYL METHYLTRANSFERASE repairs ABI-TFs and imparts desiccation tolerance in orthodox rice seeds. Development 149:dev200600. https://doi.org/10.1242/dev.200600

    Article  PubMed  Google Scholar 

  • Kamble NU, Majee M (2020) PROTEIN L-ISOASPARTYL METHYLTRANSFERASE (PIMT) in plants: Regulations and functions. Biochem J 477(22):4453–4471

    Article  CAS  Google Scholar 

  • Koornneef M, Hanhart CJ, Hilhorst HW, Karssen CM (1989) In vivo inhibition of seed development and reserve protein accumulation in recombinants of abscisic acid biosynthesis and responsiveness mutants in Arabidopsis thaliana. Plant Physiol 90(2):463–469

    Article  CAS  Google Scholar 

  • Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719

    Article  CAS  Google Scholar 

  • Kuromori T, Seo M, Shinozaki K (2018) ABA transport and plant water stress responses. Trends Plant Sci 23:513–522. https://doi.org/10.1016/j.tplants.2018.04.001

    Article  CAS  PubMed  Google Scholar 

  • McFadden PN, Clarke S (1987) Conversion of isoaspartyl peptides to normal peptides: implications for the cellular repair of damaged proteins. Proc Natl Acad Sci USA 84:2595–2599

    Article  CAS  Google Scholar 

  • Mudgett MB, Clarke S (1994) Hormonal and environmental responsiveness of a developmentally regulated protein repair L-isoaspartyl methyltransferase in wheat. J Biol Chem 269:25605–25612

    Article  CAS  Google Scholar 

  • Niu X, Helentjaris T, Bate NJ (2002) Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 14:2565–2575

    Article  CAS  Google Scholar 

  • Oge L, Bourdais G, Bove J, Collet B, Godin B, Granier F, Boutin JP, Job D, Jullien M, Grappin P (2008) Protein repair L-isoaspartyl methyltransferase 1 is involved in both seed longevity and germination vigor in Arabidopsis. Plant Cell 20:3022–3037

    Article  CAS  Google Scholar 

  • Petla BP, Kamble NU, Kumar M, Verma P, Ghosh S, Singh A, Rao V, Salvi P, Kaur H, Saxena SC, Majee M (2016) Rice PROTEIN l-ISOASPARTYL METHYLTRANSFERASE isoforms differentially accumulate during seed maturation to restrict deleterious isoAsp and reactive oxygen species accumulation and are implicated in seed vigor and longevity. New Phytol 211:627–645

    Article  CAS  Google Scholar 

  • Schardl CL, Byrd AD, Benzion G, Altschuler MA, Hildebrand DF, Hunt AG (1987) Design and construction of a versatile system for the expression of foreign genes in plants. Gene 61(1):1–11

    Article  CAS  Google Scholar 

  • Suttipanta N, Pattanaik S, Gunjan S, Xie CH, Littleton J, Yuan L (2007) Promoter analysis of the Catharanthus roseus geraniol 10-hydroxylase gene involved in terpenoid indole alkaloid biosynthesis. Biochim Biophys Acta 1769(2):139–148. https://doi.org/10.1016/j.bbaexp.2007.01.006

    Article  CAS  PubMed  Google Scholar 

  • Tian R, Wang F, Zheng Q, Niza VMGE, Downie AB, Perry SE (2020) Direct and indirect targets of the Arabidopsis seed transcription factor ABSCISIC ACID INSENSITIVE3. Plant J 103:1679–1694

    Article  CAS  Google Scholar 

  • Verma P, Kaur H, Petla BP, Rao V, Saxena SC, Majee M (2013) PROTEIN L-ISOASPARTYL METHYLTRANSFERASE2 is differentially expressed in chickpea and enhances seed vigor and longevity by reducing abnormal isoaspartyl accumulation predominantly in seed nuclear proteins. Plant Physiol 161:1141–1157

    Article  CAS  Google Scholar 

  • Wei Y, Xu H, Diao L, Zhu Y, Xie H, Cai Q, Wu F, Wang Z, Zhang J, Xie H (2015) Protein repair l-isoaspartyl methyltransferase 1 (PIMT1) in rice improves seed longevity by preserving embryo vigor and viability. Plant Mol Biol 89:475–492

    Article  CAS  Google Scholar 

  • Wind JJ, Peviani A, Snel B, Hanson J, Smeekens SC (2013) ABI4: versatile activator and repressor. Trends Plant Sci 18:125–132

    Article  CAS  Google Scholar 

  • Zinsmeister J, Lalanne D, Terrasson E, Chatelain E, Vandecasteele C, Vu BL, Dubois Laurent C, Geoffriau E, Signor CL, Dalmais M et al (2016) ABI5 is a regulator of seed maturation and longevity in legumes. Plant Cell 28:2735–2754

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grant from the Department of Biotechnology (BT/HRD/NBA/39/05/2018-19), the Government of India and core grant from the National Institute of Plant Genome Research. NUK, SG and RKA gratefully thank University Grant Commission, Council of Scientific and Industrial Research, Government of India and National Institute of Plant Genome Research for research fellowships. We gratefully thank the NIPGR confocal microscopy facility and central instrumentation facility. The authors are thankful to DBT-eLibrary Consortium (DeLCON) for providing access to e-resources.

Author information

Authors and Affiliations

  1. National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, 110067, India

    Nitin Uttam Kamble, Shraboni Ghosh, Rakesh Kumar Achary & Manoj Majee

Authors
  1. Nitin Uttam Kamble
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shraboni Ghosh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rakesh Kumar Achary
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Manoj Majee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manoj Majee.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Dorothea Bartels.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kamble, N.U., Ghosh, S., Achary, R.K. et al. Arabidopsis ABSCISIC ACID INSENSITIVE4 targets PROTEIN L-ISOASPARTYL METHYLTRANSFERASE1 in seed. Planta 256, 30 (2022). https://doi.org/10.1007/s00425-022-03947-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-022-03947-7

Keywords

Search

Navigation