Abstract
Ascorbate peroxidase (APX) is one of the important antioxidant enzymes in the active oxygen metabolism pathway of plants and animals, especially it is the key enzyme to clear H2O2 in chloroplast and the main enzyme of vitamin C metabolism. However, knowledge about APX gene family members and their evolutionary and functional characteristics in kiwifruit is limited. In this study, we identified 13 members of the APX gene family in the kiwifruit (cultivar: Hongyang) genome according the APX proteins conserved domain of Arabidopsis thaliana. Phylogenetic analysis by maximum likelihood split these 13 genes into four groups. The APX gene family members were distributed on nine chromosomes (Nos. 4, 5, 11, 13, 20, 21, 23, 25, 28). Most of the encoded hydrophilic and lipid-soluble enzymes were predicted to be located in the cytoplasm, nucleus and chloroplast. Among them, AcAPX4, AcAPX5, AcAPX8, AcAPX12 were transmembrane proteins, and AcAPX8 and AcAPX12 had the same transmembrane domain. The gene structure analysis showed that AcAPXs were composed of 4-22 introns, except that AcAPX10 was intron-free. Multiple expectation maximization for motif elicitation program (MEME) analyzed 13 APX protein sequences of Actinidia chinensis and identified 10 conserved motifs ranging in length from 15 to 50 amino acid residues. Additionally, the predicted secondary structures of the main motifs consisted of α-helix and random coils. The gene expression of fruits in different growth stages and bagging treatment were determined by qRT-PCR. The results showed that 8 AcAPXs had the highest expression levels during the color turning period and only the gene expression of AcAPX3 was consistent with the ascorbic acid content; five AcAPXs were consistent with the ascorbic acid content after bagging. Our data provided evolutionary and functional information of AcAPX gene family members and revealed the gene expression of different members in different growth stages and bagging treatments These results may be useful for future studies of the structures and functions of AcAPX family members.
Similar content being viewed by others
References
Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Sci 171:328–388. https://doi.org/10.1016/j.plantsci.2006.04.009
Ampomah DC, McGhie T, Wibisono R, Montefiori M, Hellens R, Allan AC (2009) The kiwifruit lycopene beta-cyclase plays a significant role in carotenoid accumulation in fruit. J Exp Bot 60:3765–3779. https://doi.org/10.1093/jxb/erp218
Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucl Acids Res 34(Web Server issue):W369–W373. https://doi.org/10.1093/nar/gkl198
Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis PM (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35(4 suppl 1):1011–1019. https://doi.org/10.1590/s1415-47572012000600016
Gang W, Tao W, Zhan HJ, Xuan JP, Pan DL, Guo ZR, Zhang JY (2018) Genome-wide bioinformatics analysis of MAPK gene family in Kiwifruit (Actinidia chinensis). Int J Mol Sci 19:2510. https://doi.org/10.3390/ijms19092510
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Huang SX, Ding J, Deng DJ, Tang W (2013) Draft genome of the kiwifruit Actinidia chinensis. Nature Commun 4:2640. https://doi.org/10.1038/ncomms3640
Huang CH, Ge CL, Zhang XH, Wu H, Qu XY, Xu XB (2014) Expression analysis of structural genes related to anthocyanin synthesis in a mutant of ‘Hongyang’ kiwifruit. J Fruit Sci. https://doi.org/10.13925/j.cnki.gsxb.2014.02.007
Kim MD, Kim YH, Kwon SY, Yun DJ, Kwak SS, Lee HS (2010) Enhanced tolerance to methyl viologen-induced oxidative stress and high temperature in transgenic potato plants overexpressing the CuZnSOD, APX and NDPK2 genes. Physiol Plant 140:153–162. https://doi.org/10.1111/j.1399-3054.2010.01392.x
Liao GL, He YQ, Li XS, Zhong M, Huang CH, Yi SY, Liu Q, Xu XB (2019a) Effects of bagging on fruit flavor quality and related gene expression of AsA synthesis in Actinidia eriantha. Sci Hortic 256:108511. https://doi.org/10.1016/j.scienta.2019.05.038
Liao GL, Li ZY, Huang CH, Zhong M, Tao JJ, Qu XY, Chen L, Xu Xi B (2019b) Genetic diversity of inner quality and SSR association analysis of wild kiwifruit (Actinidia eriantha). Sci Hortic 248:241–247. https://doi.org/10.1016/j.scienta.2019.01.021
Liu YJ, Yuan Y, Liu YY, Liu Y, Fu JJ, Zheng J, Wang GY (2012) Gene families of maize glutathione-ascorbate redox cycle respond differently to abiotic stresses. J Plant Physiol 169:183–192. https://doi.org/10.1016/j.jplph.2011.08.018
Ma Q (2012) Overexpression of APX gene from Populus tomentosa enhance plant tolerance to abiotic stress. Dissertation, Shandong Normal University. http://cdmd.cnki.com.cn/article/cdmd-10445-1012338529.htm
Mathews MC, Summers CB, Felton GW (1997) Ascorbate peroxidase: a novel antioxidant enzyme in insects. Archives Insect Biochem Physiol 34:57–68. https://doi.org/10.1002/(sici)1520-6327(1997)34:1%3c57:aid-arch5%3e3.0.co;2-t
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/S1360-1385(02)02312-9
Mittler R, Vanderauwera S, Gollery M, Van BF (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van BF (2011) ROS signaling: the new wave. Trends Plant Sci 16:300–309. https://doi.org/10.1016/j.tplants.2011.03.007
Najami N, Janda T, Barriah W, Kayam G, Tal M, Micha G, Volokita M (2008) Ascorbate peroxidase gene family in tomato: its identification and characterization. Mol Genet Genomics 279:171–182. https://doi.org/10.1007/s00438-007-0305-2
Narendra S, Venkataramani S, Shen GX, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H (2006) The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 57:3033–3042. https://doi.org/10.1093/jxb/erl060
Panchuk II, Volkov RA, Schoeffl F (2002) Heat stress and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129:838–853. https://doi.org/10.1104/pp.001362
Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882. https://doi.org/10.1093/jxb/erq340
Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr Opin Plant Biol 3:229–235. https://doi.org/10.1016/S1369-5266(00)80070-9
Tang L, Tang H, Kwak SS, Lee SH, Wang SY, Yang XL (2008) Improving potato plants’ oxidative stress and salt tolerance by gene transfer both of Cu/Zn superoxide dismutase and ascorbate peroxidase. China Biotechnol 28:25–31. https://doi.org/10.3969/j.issn.1671-8135.2008.03.005
Tao CC, Jin X, Zhu LP, Xie QL, Wang XC, Li HB (2018a) Genome-wide investigation and expression profiling of APX gene family in Gossypium hirsutum provide new insights in redox homeostasis maintenance during different fiber development stages. Mol Genet Genomics 293:685–697. https://doi.org/10.1007/s00438-017-1413-2
Tao JJ, Wu H, Li ZY, Huang CH, Xu XB (2018b) Molecular evolution of GDP-d-mannose epimerase (GME), a key gene in plant ascorbic acid biosynthesis. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01293
Teixeira FK, Menezes BL, Galvão VC, Margis R, Margis PM (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300–314. https://doi.org/10.1007/s00425-005-0214-8
Vandesompele J, Preter KD, Pattyn F, Poppe B, Roy NV, De Paepe A, Speleman F, Genome B (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(RESEARCH0034):1. https://doi.org/10.1186/gb-2002-3-7-research0034
Wang C, Yang CP, Wang YC (2009) Cloning and expression analysis of an APX gene from Betula platyphyla. J Northeast Forestry Univ 37(3):79–81+88
Warrington IJ, Weston GC (1990) Kiwifruit: science and management. Ray Richards Publisher. http://www.cabdirect.org/abstracts/19900397155.html
Wu H (2015) Cloning and quantitative expression of ascorbic acid synthase related genes in Actinidia eriantha. Dissertation, Jiangxi Agricultural University. http://cdmd.cnki.com.cn/Article/CDMD-10410-1015648273.htm
Xu SC, Ding HD, Sang JR (2007) Reactive oxygen species, metabolism, and signal transduction in plant cells. Acta Bot Yunnanica 29:355–365. https://doi.org/10.3969/j.issn.2095-0845.2007.03.017
Yan HH (2014) Database construction and evolutionary analysis of intronless genes in maize and related specials. Dissertation, Anhui Agricultural University. https://kns.cnki.net/kns/brief/default_result.aspx
Yao JQ, Yang SG, Chen XY, Tian SM (2018) Identification and expression of APX gene family members in Hevea brasiliensis. Genomics Appl Biol 37:4769–4774. https://doi.org/10.13417/j.gab.037.004769
Yu ZY, Ge CH, Wang XL, Xu CX, Wang QH, Cai XF (2018) Identification and expression analysis of ascorbate peroxidase gene family in spinach. J Shanghai Norm Univ 47:664–672. https://doi.org/10.3969/J.ISSN.1000-5137.2018.06.005
Yungyuen W, Ma G, Zhang L, Yamawaki KK, Yahata MK, Ohta S, Yoshioka T, Katoa M (2017) Regulation of ascorbic acid metabolism in response to different temperatures in citrus juice sacs, in vitro. Sci Hortic 217:1–7. https://doi.org/10.1016/j.scienta.2017.01.021
Zabarankin M, Uryasev S (2014) Maximum likelihood method. Springer, New York, Statistical decision problems. https://doi.org/10.1007/978-1-4614-8471-4_4
Zhang YY, Li HX, Shu WB, Zhang CJ, Ye ZB (2011) RNA interference of a mitochondrial APX gene improves vitamin C accumulation in tomato fruit. Sci Hortic 129:220–226. https://doi.org/10.1016/j.scienta.2011.03.025
Acknowledgements
This work was supported by the Project support by the National Natural Science Foundation of China (Grant nos. 31760559, 31760567), Key research and development plan of Jiangxi science and technology department (Grant no. 20192ACB60002) and the Jiangxi Provincial Construction of Kiwifruit Industry Technology System (Grant no. JXARS-05).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liao, GL., Liu, Q., Li, YQ. et al. Identification and expression profiling analysis of ascorbate peroxidase gene family in Actinidia chinensis (Hongyang). J Plant Res 133, 715–726 (2020). https://doi.org/10.1007/s10265-020-01206-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-020-01206-y