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Tree Genetics & Genomes

, 13:94 | Cite as

Identification of the SRO gene family in apples (Malus×domestica) with a functional characterization of MdRCD1

  • Haohao Li
  • Rui Li
  • Fengjia Qu
  • Jifang Yao
  • Yujin Hao
  • Xiaofei WangEmail author
  • Chunxiang YouEmail author
Original Article
Part of the following topical collections:
  1. Genome Biology

Abstract

RCD1 is a member of the plant-specific SRO protein family. Several SRO genes have been functionally identified in the regulation of abiotic stresses in Arabidopsis and other plant species. However, the function of SROs is largely unknown in apple (Malus×domestica). In this study, six MdSRO-encoding genes were isolated, categorized into two types and mapped to six chromosomes. The phylogenetic analysis demonstrated that the sequences of the AtSRO and MdSRO proteins are highly conserved. Subsequently, expression analysis showed that MdSRO genes had different expression profiles in different tissues and in response to various stresses. Finally, MdRCD1 was isolated for functional identification. The results showed that resistance to oxidation stress in apple calli was enhanced by MdRCD1 overexpression and weakened by MdRCD1 suppression. MdRCD1 also played a crucial role in the regulation of ROS homeostasis in transgenic apple calli and Arabidopsis. Ectopic expression of MdRCD1 significantly enhanced resistance to salt and oxidative stresses in transgenic lines. In addition, MdRCD1 also enhanced drought tolerance due to its influence on stomatal opening. Based on these results, we conclude that MdRCD1 is an important regulator in abiotic stress response.

Keywords

Apple SRO RCD1 Abiotic stresses 

Notes

Acknowledgements

This research was supported by grants from NSFC (31430074 and 31601742), Ministry of Education of China (IRT15R42), and Shandong Province (SDAIT-06- 03).

Author contributions

Conceived and designed the experiments: CXY XFW HHL. Performed the experiments: HHL RL. Analyzed the data: HHL RL FJQ. Contributed reagents/materials/analysis tools: YJH JFY. Wrote the paper: HHL XFW.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Data archiving statement

The apple SRO gene family sequences have been submitted to Genome Database for Rosaceae (GDR) (https://www.rosaceae.org/), and the accession number been shown in the Table 1. All sequences of A. thaliana SRO genes are available in the Arabidopsis Information Resource (TAIR) (https://www.arabidopsis.org/index.jsp)

Supplementary material

11295_2017_1175_MOESM1_ESM.docx (665 kb)
ESM 1 (DOCX 664 kb)

References

  1. Ahlfors R, Lang S, Overmyer K, Jaspers P, Brosche M, Tauriainen A, Kollist H, Tuominen H, Belles-Boix E, Piippo M, Inze D, Palva T, Kangasjarvi J (2004) Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 16:1925–1937CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ahlfors R, Brosché M, Kollist H, Kangasjärvi J (2009) Nitric oxide modulates ozone‐induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J 58(1):1–12Google Scholar
  3. Amé JC, Spenlehauer C, de Murcia G (2004) The PARP superfamily. BioEssays 26:882–893CrossRefPubMedGoogle Scholar
  4. An XH, Tian Y, Chen KQ, Wang XF, Hao YJ (2012) The apple WD40 protein MdTTG1 interacts with bHLH but not MYB proteins to regulate anthocyanin accumulation. J Plant Physiol 169(7):710–717CrossRefPubMedGoogle Scholar
  5. Aravind L (2001) The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem Sci 26:273–275CrossRefPubMedGoogle Scholar
  6. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren JY, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207CrossRefGoogle Scholar
  8. Belles-Boix E, Babiychuk E, Van Montagu M, Inze D, Kushnir S (2000) CEO1, a new protein from Arabidopsis thaliana, protects yeast against oxidative damage. FEBS Lett 482:19–24CrossRefPubMedGoogle Scholar
  9. Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123(7):1279–1291CrossRefPubMedPubMedCentralGoogle Scholar
  10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743CrossRefPubMedGoogle Scholar
  11. Dai X, Xu Y, Ma Q, Xu W, Wang T, Xue Y, Chong K (2007) Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol 143(4):1739–1751CrossRefPubMedPubMedCentralGoogle Scholar
  12. Diaz-De-Leon F, Klotz KL, Lagrimini LM (1993) Nucleotide sequence of the tobacco (Nicotiana tabacum) anionic peroxidase gene. Plant Physiol 101(3):1117CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dolferus R, Jacobs M, Peacock WJ, Dennis ES (1994) Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol 105(4):1075–1087CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fitter DW, Martin DJ, Copley MJ, Scotland RW, Langdale JA (2002) GLK gene pairs regulate chloroplast development in diverse plant species. Plant J 31(6):713–727CrossRefPubMedGoogle Scholar
  15. Fujibe T, Saji H, Arakawa K, Yabe N, Takeuchi Y, Yamamoto KT (2004) A methyl viologen-resistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental ultraviolet-B irradiation. Plant Physiol 134:275–285CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48:909–930CrossRefGoogle Scholar
  17. Hassa PO, Hottiger MO (2008) The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front Biosci 13:3046–3082CrossRefPubMedGoogle Scholar
  18. Hassa PO, Haenni SS, Elser M, Hottiger MO (2006) Nuclear ADPribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol Mol Biol Rev 70:789–829CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hobo T, Asada M, Kowyama Y, Hattori T (1999) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19(6):679–689CrossRefPubMedGoogle Scholar
  20. Jaspers P, Blomster T, Brosché M, Salojärvi J, Ahlfors R, Vainonen JP, Reddy RA, Immink R, Angenent G, Turck F, Overmyer K, Kangasjärvi J (2009) Unequally redundant RCD1 and SRO1 mediate stress and developmental responses and interact with transcription factors. Plant J 60(2):268–279Google Scholar
  21. Jaspers P, Overmyer K, Wrzaczek M, Vainonen JP, Blomster T, Salojärvi J, Reddy RO, Kangasjärvi J (2010) The RST and PARP-like domain containing SRO protein family: analysis of protein structure, function and conservation in land plants. BMC Genomics 11(1):1CrossRefGoogle Scholar
  22. Katiyar-Agarwal S, Zhu J, Kim K, Agarwal M, Fu X, Huang A, Zhu JK (2006) The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:18816–18821CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kim MY, Zhang T, Kraus WL (2005) Poly (ADP-ribosyl) ation by PARP-1: ‘PAR-laying’ NAD+ into a nuclear signal. Genes Dev 19:1951–1967CrossRefPubMedGoogle Scholar
  24. Kjaersgaard T, Jensen MK, Christiansen MW, Gregersen P, Kragelund BB, Skriver K (2011) Senescence-associated barley NAC (NAM, ATAF1, 2, CUC) transcription factor interacts with radical-induced cell death 1 through a disordered regulatory domain. J Biol Chem 286(41):35418–35429CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35(1):53–60CrossRefPubMedGoogle Scholar
  26. Li W, Cui X, Meng Z, Huang X, Xie Q, Wu H, Jin H, Zhang D, Liang W (2012) Transcriptional regulation of Arabidopsis MIR168a and argonaute1 homeostasis in abscisic acid and abiotic stress responses. Plant Physiol 158(3):1279–1292CrossRefPubMedPubMedCentralGoogle Scholar
  27. Liu S, Liu S, Wang M, Wei T, Meng C, Wang M, Xia G (2014) A wheat SIMILAR TO RCD-ONE gene enhances seedling growth and abiotic stress resistance by modulating redox homeostasis and maintaining genomic integrity. Plant Cell 26(1):164–180CrossRefPubMedPubMedCentralGoogle Scholar
  28. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefPubMedGoogle Scholar
  29. Otto H, Reche PA, Bazan F, Dittmar K, Haag F, Koch-Nolte F (2005) In silico characterization of the family of PARP-like poly(ADP-ribosyl) transferases (pARTs). BMC Genomics 6:139CrossRefPubMedPubMedCentralGoogle Scholar
  30. Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H, Kangasjärvi J (2000) Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12(10):1849–1862Google Scholar
  31. Petrov VD, Van Breusegem F (2012) Hydrogen peroxide—a central hub for information flow in plant cells. AoB plants pls014Google Scholar
  32. Romero-Puertas MC, Rodríguez-Serrano M, Corpas FJ, Gomez MD, Del Rio LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O2·− and H2O2 in pea leaves. Plant Cell Environ 27(9):1122–1134CrossRefGoogle Scholar
  33. Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly (ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517–528CrossRefPubMedGoogle Scholar
  34. Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410(6826):327–330CrossRefPubMedGoogle Scholar
  35. Sievers F, Higgins DG (2014) Clustal omega, accurate alignment of very large numbers of sequences. Methods Mol Biol 1079:105–116CrossRefPubMedGoogle Scholar
  36. Singh KB, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5(5):430–436CrossRefPubMedGoogle Scholar
  37. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270CrossRefPubMedGoogle Scholar
  38. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) Mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(4):2725e2729Google Scholar
  39. Tang ZC (1999) Modern experiment procotols in plant physiologyGoogle Scholar
  40. Teotia S, Lamb RS (2009) The paralogous genes RADICAL-INDUCED CELL DEATH1 and SIMILAR TO RCD ONE1 have partially redundant functions during Arabidopsis development. Plant Physiol 151(1):180–198CrossRefPubMedPubMedCentralGoogle Scholar
  41. Vainonen JP, Jaspers P, Wrzaczek M, Lamminmäki A, Reddy RA, Vaahtera L, Brosche M, Kangasjärvi J (2012) RCD1–DREB2A interaction in leaf senescence and stress responses in Arabidopsis thaliana. Biochem J 442(3):573–581CrossRefPubMedGoogle Scholar
  42. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A et al (2010) The genome of the domesticated apple (Malus×domestica Borkh.) Nat Genet 42(10):833–839CrossRefPubMedGoogle Scholar
  43. Wardhan V, Jahan K, Gupta S, Chennareddy S, Datta A, Chakraborty S, Chakraborty N (2012) Overexpression of CaTLP1, a putative transcription factor in chickpea (Cicer arietinum L.), promotes stress tolerance. Plant Mol Biol 79(4-5):479–493Google Scholar
  44. Wrzaczek M, Brosché M, Kangasjärvi J (2013) ROS signaling loops—production, perception, regulation. Curr Opin Plant Biol 16:575–582CrossRefPubMedGoogle Scholar
  45. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(suppl 1):S165–S183PubMedPubMedCentralGoogle Scholar
  46. You J, Zong W, Li X, Ning J, Hu H, Li X, Xiao J, Xiong L (2013) The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J Exp Bot 64(2):569–583Google Scholar
  47. Zweifel ME, Leahy DJ, Barrick D (2005) Structure and Notch receptor binding of the tandem WWE domain of Deltex. Structure 13:1599–1611CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Haohao Li
    • 1
    • 2
    • 3
  • Rui Li
    • 1
    • 2
    • 3
  • Fengjia Qu
    • 1
    • 2
    • 3
  • Jifang Yao
    • 1
    • 2
    • 3
  • Yujin Hao
    • 1
    • 2
    • 3
  • Xiaofei Wang
    • 1
    • 2
    • 3
    Email author
  • Chunxiang You
    • 1
    • 2
    • 3
    Email author
  1. 1.National Key Laboratory of Crop BiologyShandong Agricultural UniversityTai-AnChina
  2. 2.National Research Center for Apple Engineering and TechnologyShandong Agricultural UniversityTai-AnChina
  3. 3.College of Horticulture Science and EngineeringShandong Agricultural UniversityTai-AnChina

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