Abstract
Key message
Superoxide dismutase genes were expressed differentially along with developmental stages of fertilized ovules in Xanthoceras sorbifolium, and the XsMSD gene silencing resulted in the arrest of fertilized ovule development.
Abstract
A very small percentage of mature fruits (ca. 5%) are produced relative to the number of bisexual flowers in Xanthoceras sorbifolium because seeds and fruits are aborted at early stages of development after pollination. Reactive oxygen species (ROS) in plants are implicated in an extensive range of biological processes, such as programmed cell death and senescence. Superoxide dismutase (SOD) activity might be required to regulate ROS homeostasis in the fertilized ovules of X. sorbifolium. The present study identified five SOD genes and one SOD copper chaperone gene in the tree. Their transcripts were differentially expressed along different stages of fertilized ovule development. These genes showed maximum expression in the ovules at 3 days after pollination (DAP), a time point in which free nuclear endosperm and nucleus tissues rapidly develop. The XsCSD1, XsFSD1 and XsMSD contained seven, eight, and five introns, respectively. Analysis of the 5′-flanking region of XsFSD1 and XsMSD revealed many cis-acting regulatory elements. Evaluation of XsMSD gene function based on virus-induced gene silencing (VIGS) indicated that the gene was closely related to early development of the fertilized ovules and fruits. This study suggested that SOD genes might be closely associated with the fate of ovule development (aborted or viable) after fertilization in X. sorbifolium.
Similar content being viewed by others
References
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gel. Anal Biochem 44:276–287
Chu CC, Lee WC, Guo WY, Pan SM, Chen LJ, Li HM, Jinn TL (2005) A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis. Plant Physiol 139:425–436. https://doi.org/10.1104/pp.105.065284
Cohu CM, Abdel-Ghany SE, Gogolin Reynolds KA, Onofrio AM, Bodecker JR, Kimbrel JA, Niyogi KK, Pilon M (2009) Copper delivery by the copper chaperone for chloroplast and cytosolic copper/zinc-superoxide dismutases: regulation and unexpected phenotypes in an Arabidopsis mutant. Mol Plant 2:1336–1350. https://doi.org/10.1093/mp/ssp084
Fink RC, Scandalios JG (2002) Molecular evolution and structure–function relationships of the superoxide dismutase gene families in angiosperms and their relationship to other eukaryotic and prokaryotic superoxide dismutases. Arch Biochem Biophys 399:19–36
Forman HJ, Fridovich I (1973) On the stability of bovine superoxide dismutase: the effects of metals. J Biol Chem 248:2645–2649
Glerum DM, Shtanko A, Tzagoloff A (1996) Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J Biol Chem 271:14504–14509
Gupta DK, Pena LB, Romero-Puertas MC, Hernández A, Inouhe M, Sandalio LM (2017) NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity. Plant Cell Environ 40:509–526
Horecka J, Kinsey PT, Sprague GFJ (1995) Cloning and characterization of the Saccharomyces cerevisiae LYS7 gene: evidence for function outside of lysine biosynthesis. Gene 162:7–92
Huang CH, Kuo WY, Weiss C, Jinn TL (2012) Copper chaperone-dependent and -independent activation of three copper–zinc superoxide dismutase homologs localized in different cellular compartments in Arabidopsis. Plant Physiol 158:737–746. https://doi.org/10.1104/pp.111.190223
Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118:637–650
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163. https://doi.org/10.1093/bib/5.2.150
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327. https://doi.org/10.1093/nar/30.1.325
Li W, Qi L, Lin X, Chen H, Ma Z, Wu K, Huang S (2009) The expression of manganese superoxide dismutase gene from Nelumbo nucifera responds strongly to chilling and oxidative stresses. J Integr Plant Biol 51:279–286. https://doi.org/10.1111/j.1744-7909.2008.00790.x
Lin YL, Lai ZX (2013) Superoxide dismutase multigene family in longan somatic embryos: a comparison of CuZn-SOD, Fe-SOD, and Mn-SOD gene structure, splicing, phylogeny, and expression. Mol Breed 32:595–615. https://doi.org/10.1007/s11032-013-9892-2
Lin SJ, Pufahl RA, Dancis A, O’Halloran TV, Culotta VC (1997) A role for the Saccharomyces cerevisiae ATX1 gene in copper trafficking and iron transport. J Biol Chem 272:9215–9220
Lu D, Wang T, Persson S, Mueller-Roeber B, Schippers JHM (2014) Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development. Nat Commun 5:3767. https://doi.org/10.1038/ncomms4767
María VM, Diego FF, Venkatesan S, Eduardo JZ, Gabriela CP (2013) Oiwa, a female gametophytic mutant impaired in a mitochondrial manganese-superoxide dismutase, reveals crucial roles for reactive oxygen species during embryo sac development and fertilization in Arabidopsis. Plant Cell 25:1573–1591. https://doi.org/10.1105/tpc.113.109306
McCord JM, Fridovich I (1988) Superoxide dismutase: the first twenty years (1968–1988). Free Radic Biol Med 5:363–369
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K et al (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309. https://doi.org/10.1016/j.tplants.2011.03.007
Momcilovic I, Pantelic D, Hfidan M, Savic J, Vinterhalter D (2014) Improved procedure for detection of superoxide dismutase isoforms in potato, Solanum tuberosum L. Acta Physiol Plant 36:2059–2066. https://doi.org/10.1007/s11738-014-1583-z
Moran JF, James EK, Rubio MC, Sarath G, Klucas RV, Becana M (2003) Functional characterization and expression of a cytosolic iron-superoxide dismutase from cowpea root nodules. Plant Physiol 133:773–782. https://doi.org/10.1104/pp.103.023010
Pan SM, Hwang GB, Liu HC (1999) Over-expression and characterization of copper/zinc-superoxide dismutase from rice in Escherichia coli. Bot Bull Acad Sin (Taipei) 40:275–281
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, del Rio LA (2013) Role of peroxisomes as a source of reactive oxygen species (ROS) signalling molecules. Subcell Biochem 69:231–255. https://doi.org/10.1007/978-94-007-6889-5_13
Singh R, Singh S, Parihar P, Mishra RK, Tripathi DK, Singh VP, Chauhan DK, Prasad SM (2016) Reactive oxygen species (ROS): beneficial companions of plants’ developmental processes. Front Plant Sci 7:1299. https://doi.org/10.3389/fpls.2016.01299
Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43
Srivalli B, Khanna-Chopra R (2001) Induction of new isoforms of superoxide dismutase and catalase enzymes in the flag leaf of wheat during monocarpic senescence. Biochem Biophys Res Commun 288:1037–1042. https://doi.org/10.1006/bbrc.2001.5843
Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270. https://doi.org/10.1111/j.1365-3040.2011.02336.x
Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616. https://doi.org/10.1016/j.cell.2010.10.020
Van Camp W, Bowler C, Villarroel R, Tsang EWT, Van Montagu M, Inze D (1990) Characterization of iron superoxide dismutase cDNAs from plants obtained by genetic complementation in Escherichia coli. Proc Natl Acad Sci USA 87:9903–9907
Wang Y, Ying Y, Chen J, Wang X (2004) Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Sci 167:671–677. https://doi.org/10.1016/j.plantsci.2004.03.032
White JA, Scandalios G (1988) Isolation and characterization of a cDNA for mitochondrial manganese superoxide dismutase (SOD-3) of maize and its relation to other manganese superoxide dismutase. Biochem Biophys Acta 951:61–70
Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–552
Zhou QY, Liu GS (2012) The embryology of Xanthoceras and its phylogenetic implications. Plant Syst Evol 298:457–468. https://doi.org/10.1007/s00606-011-0558-4
Zhou QY, Zheng YR (2015) Comparative de novo transcriptome analysis of fertilized ovules in Xanthoceras sorbifolium uncovered a pool of genes expressed specifically or preferentially in the selfed ovule that are potentially involved in late-acting self-incompatibility. PLOS One 10:e0140507. https://doi.org/10.1371/journal.pone.0140507
Zhou QY, Zheng YR, Lai LM, Du H (2017) Observations on sexual reproduction in Xanthoceras sorbifolium (Sapindaceae). Acta Bot Occident Sin 37:0014–0022. https://doi.org/10.7606/j.issn.1000-4025.2017.01.0014
Acknowledgements
We would like to thank Jie Wen and Fengqin Dong for technical help. This work was supported by the National Natural Science Foundation of China (30972344, 31370611 and 31570680) and Beijing Natural Science Foundation (6172028).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Qiaochun Wang.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhou, Q., Cai, Q. The superoxide dismutase genes might be required for appropriate development of the ovule after fertilization in Xanthoceras sorbifolium. Plant Cell Rep 37, 727–739 (2018). https://doi.org/10.1007/s00299-018-2263-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-018-2263-z