Citation: | Sun LJ,Liu TL,Liu H,Yuan DY,Yang XL,Xu YS,Chen SY,Zeng JG,Huang YB,Tan YN. Effect of ascorbic acid oxidation inhibition on growth of Oryza sativa L. seedlings under abscisic acid (ABA) treatment[J]. Plant Science Journal,2024,42(6):806−814. DOI: 10.11913/PSJ.2095-0837.23378 |
Ascorbic acid (AsA) oxidation is a critical biological process involved in maintaining ascorbic acid homeostasis. However, its regulation by abscisic acid (ABA) and associated biological effects remain unknown. This study selected OsAAO4, an ascorbate oxidase gene in rice (Oryza sativa L.), to analyze its response to ABA and the phenotypic and physiological effects of its knockout under ABA treatment. Results showed that OsAAO4 contained abundant ABA response elements and reached peak expression levels in roots and young leaves after 9 h of ABA treatment, increasing 13.8-fold and 7.4-fold, respectively. Under normal conditions without ABA treatment, there were no significant differences in plant height and survival rate between the wild-type (‘Zhonghua 11’) and OsAAO4 knockout lines (KO-1 and KO-2). However, exposure to 10 μmol/L ABA resulted in significant reductions in plant height (38.34% in KO-1 and 25.72% in KO-2) and survival rate (21.91% in KO-1 and 5.48% in KO-2) compared to wild-type rice. Additionally, in young leaves, the knockout lines exhibited decreased ascorbic acid oxidase (AAO) activity (35.31% in KO-1 and 31.81% in KO-2) and dehydroascorbic acid (DHA) content (29.72% in KO-1 and 26.95% in KO-2), while AsA content increased (27.17% in KO-1 and 16.37% in KO-2). Transcriptomic analysis revealed that differentially expressed genes (DEGs) between KO-1 and wild-type rice under ABA treatment were significantly enriched in pathways involved in redox homeostasis and oxidative stress. These findings suggest that ascorbic acid oxidation mediated by OsAAO4 plays an important role in maintaining AsA homeostasis and ensuring the normal growth of rice seedlings under ABA treatment.
[1] |
Rong L,Xin S,Tao CC,Jin X,Li HB. Cotton ascorbate oxidase promotes cell growth in cultured tobacco bright yellow-2 cells through generation of apoplast oxidation[J]. Int J Mol Sci,2017,18(7):1346 doi: 10.3390/ijms18071346
|
[2] |
Guo ZF,Tan HQ,Zhu ZH,Lu SY,Zhou BY. Effect of intermediates on ascorbic acid and oxalate biosynthesis of rice and in relation to its stress resistance[J]. Plant Physiol Biochem,2005,43(10-11):955−962. doi: 10.1016/j.plaphy.2005.08.007
|
[3] |
Smirnoff N,Wheeler GL. Ascorbic acid in plants:biosynthesis and function[J]. Crit Rev Biochem Mol Biol,2000,35(4):291−314. doi: 10.1080/10409230008984166
|
[4] |
Gallie DR. The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth[J]. J Exp Bot,2013,64(2):433−443. doi: 10.1093/jxb/ers330
|
[5] |
De Tullio MC,Liso R,Arrigoni O. Ascorbic acid oxidase:an enzyme in search of a role[J]. Biol Plantarum,2004,48(2):161−166. doi: 10.1023/B:BIOP.0000033439.34635.a6
|
[6] |
Pignocchi C,Fletcher JM,Wilkinson JE,Barnes JD,Foyer CH. The function of ascorbate oxidase in tobacco[J]. Plant Physiol,2003,132(3):1631−1641. doi: 10.1104/pp.103.022798
|
[7] |
Fotopoulos V,Sanmartin M,Kanellis AK. Effect of ascorbate oxidase over-expression on ascorbate recycling gene expression in response to agents imposing oxidative stress[J]. J Exp Bot,2006,57(14):3933−3943. doi: 10.1093/jxb/erl147
|
[8] |
Batth R,Singh K,Kumari S,Mustafiz A. Transcript profiling reveals the presence of abiotic stress and developmental stage specific ascorbate oxidase genes in plants[J]. Front Plant Sci,2017,8:198.
|
[9] |
Zechmann B. Subcellular distribution of ascorbate in plants[J]. Plant Signal Behav,2011,6(3):360−363. doi: 10.4161/psb.6.3.14342
|
[10] |
Ueda Y,Siddique S,Frei M. A novel gene,OZONE-RESPONSIVE APOPLASTIC PROTEIN1,enhances cell death in ozone stress in rice[J]. Plant Physiol,2015,169(1):873−889. doi: 10.1104/pp.15.00956
|
[11] |
Hu JX,Liu MX,Zhang A,Dai Y,Chen WZ,et al. Co-evolved plant and blast fungus ascorbate oxidases orchestrate the redox state of host apoplast to modulate rice immunity[J]. Mol Plant,2022,15(8):1347−1366. doi: 10.1016/j.molp.2022.07.001
|
[12] |
Singh RR,Verstraeten B,Siddique S,Tegene AM,Tenhaken R,et al. Ascorbate oxidation activates systemic defence against root-knot nematode Meloidogyne graminicola in rice[J]. J Exp Bot,2020,71(14):4271−4284. doi: 10.1093/jxb/eraa171
|
[13] |
童超. ABA生理功能与信号转导相关综述[J]. 科技资讯,2008(10):44−45. doi: 10.3969/j.issn.1672-3791.2008.10.037
|
[14] |
Teng KQ,Li JZ,Liu L,Han YC,Du YX,et al. Exogenous ABA induces drought tolerance in upland rice:the role of chloroplast and ABA biosynthesis-related gene expression on photosystem Ⅱ during PEG stress[J]. Acta Physiol Plant,2014,36(8):2219−2227. doi: 10.1007/s11738-014-1599-4
|
[15] |
Sanmartin M,Pateraki I,Chatzopoulou F,Kanellis AK. Differential expression of the ascorbate oxidase multigene family during fruit development and in response to stress[J]. Planta,2007,225(4):873−885. doi: 10.1007/s00425-006-0399-5
|
[16] |
Postiglione AE,Muday GK. The role of ROS homeostasis in ABA-induced guard cell signaling[J]. Front Plant Sci,2020,11:968. doi: 10.3389/fpls.2020.00968
|
[17] |
Farvardin A,González-Hernández AI,Llorens E,García-Agustín P,Scalschi L,et al. The apoplast:a key player in plant survival[J]. Antioxidants,2020,9(7):604. doi: 10.3390/antiox9070604
|
[18] |
Rogalla H,Römheld V. Role of leaf apoplast in silicon-mediated manganese tolerance of Cucumis sativus L.[J]. Plant Cell Environ,2002,25(4):549−555. doi: 10.1046/j.1365-3040.2002.00835.x
|
[19] |
Li JJ,Li Y,Yin ZG,Jiang JH,Zhang MH,et al. OsASR5 enhances drought tolerance through a stomatal closure pathway associated with ABA and H2O2 signalling in rice[J]. Plant Biotechnol J,2017,15(2):183−196.
|
[20] |
Söderman EM,Brocard IM,Lynch TJ,Finkelstein RR. Regulation and function of the Arabidopsis ABA-insensitive4 gene in seed and abscisic acid response signaling networks[J]. Plant Physiol,2000,124(4):1752−1765. doi: 10.1104/pp.124.4.1752
|
[21] |
Finkelstein RR,Lynch TJ. The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor[J]. Plant Cell,2000,12(4):599−609. doi: 10.1105/tpc.12.4.599
|
[22] |
Finkelstein RR,Somerville CR. Three classes of abscisic acid (ABA)-insensitive mutations of Arabidopsis define genes that control overlapping subsets of ABA responses[J]. Plant Physiol,1990,94(3):1172−1179. doi: 10.1104/pp.94.3.1172
|
[23] |
Yang C,Li XB,Chen SQ,Liu CL,Yang LM,et al. ABI5-FLZ13 module transcriptionally represses growth-related genes to delay seed germination in response to ABA[J]. Plant Commun,2023,4(6):100636. doi: 10.1016/j.xplc.2023.100636
|
[24] |
Liso R,De Tullio MC,Ciraci S,Balestrini R,La Rocca N,et al. Localization of ascorbic acid,ascorbic acid oxidase,and glutathione in roots of Cucurbita maxima L.[J]. J Exp Bot,2004,55(408):2589−2597. doi: 10.1093/jxb/erh262
|
[25] |
Yamamoto A,Bhuiyan NH,Waditee R,Tanaka Y,Esaka M,et al. Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants[J]. J Exp Bot,2005,56(417):1785−1796. doi: 10.1093/jxb/eri167
|
[26] |
Wang M,Guo WP,Li J,Pan XJ,Pan LH,et al. The miR528-AO module confers enhanced salt tolerance in rice by modulating the ascorbic acid and abscisic acid metabolism and ROS scavenging[J]. J Agric Food Chem,2021,69(31):8634−8648. doi: 10.1021/acs.jafc.1c01096
|
[27] |
Chen Z,Gallie DR. Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance[J]. Plant Physiol,2005,138(3):1673−1689. doi: 10.1104/pp.105.062000
|
[28] |
Chatzopoulou F,Sanmartin M,Mellidou I,Pateraki I,Koukounaras A,et al. Silencing of ascorbate oxidase results in reduced growth,altered ascorbic acid levels and ripening pattern in melon fruit[J]. Plant Physiol Biochem,2020,156:291−303. doi: 10.1016/j.plaphy.2020.08.040
|
[29] |
Wang GF,Li WQ,Li WY,Wu GL,Zhou CY,et al. Characterization of rice NADPH oxidase genes and their expression under various environmental conditions[J]. Int J Mol Sci,2013,14(5):9440−9458. doi: 10.3390/ijms14059440
|