Research Progress of Proton Pumps and Their Regulation in Organic Acid Accumulation in Horticultural Plants

doi:10.16420/j.issn.0513-353x.2021-0936

Acta Horticulturae Sinica ›› 2022, Vol. 49 ›› Issue (12): 2611-2621.doi: 10.16420/j.issn.0513-353x.2021-0936

• Reviews • Previous Articles Next Articles

Research Progress of Proton Pumps and Their Regulation in Organic Acid Accumulation in Horticultural Plants

SHI Caiyun¹, LIU Li¹, WEI Zhifeng¹, GAO Dengtao¹^,^*(), LIU Yongzhong²^,^*()

¹Zhengzhou Fruit Tree Research Institute，Chinese Academy of Agricultural Sciences，Zhengzhou 450009，China
²Key Laboratory of Horticultural Plant Biology（Ministry of Education），College of Horticulture & Forestry Sciences，Huazhong Agricultural University，Wuhan 430070，China

Received:2022-06-07 Revised:2022-08-25 Online:2022-12-25 Published:2023-01-02
Contact: GAO Dengtao,LIU Yongzhong E-mail:gaodengtao@caas.cn;liuyongzhong@mail.hzau.edu.cn

Abstract

Abstract:

Proton pumps are types of important enzymes that promote proton（H⁺）transmembrane transport and cause potential difference between the membrane and participate in a variety of life processes. Organic acids are mainly stored in vacuoles and proton pump promotes proton transmembrane transport accompanied by energy release，which then provides power for the transmembrane transport and storage of organic acids in vacuoles. This paper focuses on the categories，structural characteristics and regulatory factors of proton pumps related to acid transport in horticultural plants，as well as the research status of different types of proton pumps in the regulation of organic acid accumulation，in order to provide reference for the research and regulation of proton pumps and organic acid accumulation in horticultural plants，and then provide a theoretical basis for regulating the quality of horticultural plants.

Key words: horticultural plant, organic acid, proton pump, fruit, regulating of quality

CLC Number:

S6
Q 945

SHI Caiyun, LIU Li, WEI Zhifeng, GAO Dengtao, LIU Yongzhong. Research Progress of Proton Pumps and Their Regulation in Organic Acid Accumulation in Horticultural Plants[J]. Acta Horticulturae Sinica, 2022, 49(12): 2611-2621.

Figures/Tables 2

References 94

[1]	Amemiya T. 2005. Enhancement of vacuolar H⁺-ATPase and H⁺-pyrophosphatase expression by phytohormones in pear fruit. Journal of Japanese Society for Horticultural Sciences, 74 (5):353-360.
[2]	Aprile A, Federici C, Close T J, de Bellis L, Cattivelli L, Roose M L. 2011. Expression of the H⁺-ATPase AHA 10 proton pump is associated with citric acid accumulation in lemon juice sac cells. Functional & Integrative Genomics, 11 (4):551-563.
[3]	Axelsen K B, Palmgren M G. 2001. Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiology, 126 (2):696-706. pmid: 11402198
[4]	Azevedo I G, Oliveira J G, da Silva M G, Pereira T, Corrêa S F, Vargas H, Façanha A R. 2008. P-type H⁺-ATPases activity,membrane integrity,and apoplastic pH during papaya fruit ripening. Postharvest Biology and Technology, 48 (2):242-247. doi: 10.1016/j.postharvbio.2007.11.001 URL
[5]	Batelli G, Verslues P E, Agius F, Qiu Q, Fujii H, Pan S, Schumaker K S, Grillo S, Zhu J K. 2007. SOS 2 promotes salt tolerance in part by interacting with the vacuolar H⁺-ATPase and upregulating its transport activity. Molecular and Cellular Biology, 27 (22):7781-7790. doi: 10.1128/MCB.00430-07 URL
[6]	Baxter I, Tchieu J, Sussman M R, Boutry M, Palmgren M G, Gribskov M, Harper J F, Axelsen K B. 2003. Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiology, 132 (2):618-628. pmid: 12805592
[7]	Binzel M L. 1995. NaCl-induced accumulation of tonoplast and plasma membrane H⁺-ATPase message in tomato. Physiologia Plantarum, 94 (4):722-728. doi: 10.1111/j.1399-3054.1995.tb00990.x URL
[8]	Brune A, Müller M, Taiz L, Gonzalez P, Etxeberria E. 2002. Vacuolar acidification in citrus fruit:comparison between acid lime(Citrus aurantifolia)and sweet lime(Citrus limmetioides)juice cells. Journal of the American Society for Horticultural Science, 127 (2):171-177. doi: 10.21273/JASHS.127.2.171 URL
[9]	Brux A, Liu T Y, Krebs M, Stierhof Y D, Lohmann J U, Miersch O, Wasternack C, Schumacher K. 2008. Reduced V-ATPase activity in the trans-Golgi network causes oxylipin-dependent hypocotyl growth inhibition in Arabidopsis. Plant Cell, 20 (4):1088-1100. doi: 10.1105/tpc.108.058362 URL
[10]	Buch-Pedersen M J, Pedersen B P, Veierskov B, Nissen P, Palmgren M G. 2009. Protons and how they are transported by proton pumps. Pflügers Archiv-European Journal of Physiology, 457 (3):573-579. doi: 10.1007/s00424-008-0503-8 URL
[11]	Cipriano D J, Wang Y, Bond S, Hinton A, Jefferies K C, Qi J, Forgac M. 2008. Structure and regulation of the vacuolar ATPases. Biochimica et Biophysica Acta, 1777 (7-8):599-604. doi: 10.1016/j.bbabio.2008.03.013 pmid: 18423392
[12]	Coker J S, Jones D, Davies E. 2003. Identification,conservation,and relative expression of V-ATPase cDNAs in tomato plants. Plant Molecular Biology Reporter, 21 (2):145-158. doi: 10.1007/BF02774241 URL
[13]	Dettmer J, Hong-Hermesdorf A, Stierhof Y D, Schumacher K. 2006. Vacuolar H⁺-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. The Plant Cell, 18 (3):715-730. doi: 10.1105/tpc.105.037978 URL
[14]	Dietz K J, Tavakoli N, Kluge C, Mimura T, Sharma S, Harris G, Chardonnens A, Golldack D. 2001. Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. Journal of Experimental Botany, 52 (363):1969-1980. doi: 10.1093/jexbot/52.363.1969 pmid: 11559732
[15]	Dong Q L, Liu D D, An X H, Hu D G, Yao Y X, Hao Y J. 2011. MdVHP 1 encodes an apple vacuolar H⁺-PPase and enhances stress tolerance in transgenic apple callus and tomato. Journal of Plant Physiology, 168 (17):2124-2133. doi: 10.1016/j.jplph.2011.07.001 URL
[16]	Dong Q L, Wang C R, Liu D D, Hu D G, Fang M J, You C X, Yao Y X, Hao Y J. 2013. MdVHA-A encodes an apple subunit A of vacuolar H⁺-ATPase and enhances drought tolerance in transgenic tobacco seedlings. Journal of Plant Physiology, 170 (6):601-609. doi: 10.1016/j.jplph.2012.12.014 URL
[17]	Drozdowicz Y M, Rea P A. 2001. Vacuolar H⁺-pyrophosphatases:from the evolutionary backwaters into the mainstream. Trends in Plant Science, 6 (5):206-211. pmid: 11335173
[18]	Duby G, Boutry M. 2009. The plant plasma membrane proton pump ATPase:a highly regulated P-type ATPase with multiple physiological roles. Pflügers Archiv-European Journal of Physiology, 457 (3):645-655. doi: 10.1007/s00424-008-0457-x URL
[19]	Etienne A, Genard M, Lobit P, Mbeguie A M D, Bugaud C. 2013. What controls fleshy fruit acidity? A review of malate and citrate accumulation in fruit cells. Journal of Experimental Botany, 64 (6):1451-1469. doi: 10.1093/jxb/ert035 pmid: 23408829
[20]	Etienne C, Moing A, Dirlewanger E, Raymond P, Monet R, Rothan C. 2002a. Isolation and characterization of six peach cDNAs encoding key proteins in organic acid metabolism and solute accumulation:involvement in regulating peach fruit acidity. Physiologia Plantarum, 114 (2):259-270. doi: 10.1034/j.1399-3054.2002.1140212.x URL
[21]	Etienne C, Rothan C, Moing A, Plomion C, Bodénès C, Svanella-Dumas L, Cosson P, Pronier V, Monet R, Dirlewanger E. 2002b. Candidate genes and QTLs for sugar and organic acid content in peach [Prunus persica (L.) Batsch]. Theoretical & Applied Genetics, 105 (1):145-159.
[22]	Ewing N N, Bennett A B. 1994. Assessment of the number and expression of P-type H⁺-ATPase genes in tomato. Plant Physiology, 106 (2):547-557. doi: 10.1104/pp.106.2.547 pmid: 7991683
[23]	Falhof J, Pedersen J T, Fuglsang A T, Palmgren M. 2016. Plasma membrane H⁺-ATPase regulation in the center of plant physiology. Molecular Plant, 9 (3):323-337. doi: S1674-2052(15)00427-X pmid: 26584714
[24]	Faraco M, Spelt C, Bliek M, Verweij W, Hoshino A, Espen L, Prinsi B, Jaarsma R, Tarhan E, de Boer A H, Di Sansebastiano G P, Koes R, Quattrocchio F M. 2014. Hyperacidification of vacuoles by the combined action of two different P-ATPases in the tonoplast determines flower color. Cell Report, 6 (1):32-43.
[25]	Ferjani A, Segami S, Horiguchi G, Muto Y, Maeshima M, Tsukaya H. 2011. Keep an Eye on PPi:the vacuolar-type H⁺-pyrophosphatase regulates postgerminative development in Arabidopsis. The Plant Cell, 23 (8):2895-2908. doi: 10.1105/tpc.111.085415 pmid: 21862707
[26]	Fukuda A, Tanaka Y. 2006. Effects of ABA,auxin,and gibberellin on the expression of genes for vacuolar H⁺-inorganic pyrophosphatase,H⁺-ATPase subunit A,and Na⁺/H⁺ antiporter in barley. Plant Physiology and Biochemistry, 44 (5):351-358. doi: 10.1016/j.plaphy.2006.06.012 URL
[27]	Gaxiola R A, Palmgren M G, Schumacher K. 2007. Plant proton pumps. FEBS Letters, 581 (12):2204-2214. doi: 10.1016/j.febslet.2007.03.050 pmid: 17412324
[28]	Guo L X, Shi C Y, Liu X, Ning D Y, Jing L F, Yang H, Liu Y Z. 2016. Citrate accumulation-related gene expression and/or enzyme activity analysis combined with metabolomics provide a novel insight for an orange mutant. Scientific Reports,629343.
[29]	Hosaka M, Kanayama Y, Shiratake K, Yamaki S. 1994. Tonoplast H⁺-ATPase of mature pear fruit. Phytochemistry, 36 (3):565-567. doi: 10.1016/S0031-9422(00)89775-7 URL
[30]	Hu D G, Li Y Y, Zhang Q Y, Li M, Sun C H, Yu J Q, Hao Y J. 2017. R2R3-MYB transcription factor MdMYB 73 is involved in malate accumulation and vacuolar acidification in apple. Plant Journal, 91 (3):443-454. doi: 10.1111/tpj.13579 URL
[31]	Hu D G, Sun C H, Ma Q J, You C X, Cheng L, Hao Y J. 2016a. MdMYB 1 regulates anthocyanin and malate accumulation by directly facilitating their transport into vacuoles in apples. Plant Physiology, 170 (3):1315-1330. doi: 10.1104/pp.15.01333 URL
[32]	Hu D G, Sun C H, Sun M H, Hao Y J. 2016b. MdSOS2L1 phosphorylates MdVHA-B1 to modulate malate accumulation in response to salinity in apple. Plant Cell Reports, 35 (3):705-718. doi: 10.1007/s00299-015-1914-6 URL
[33]	Hu D G, Sun M H, Sun C H, Liu X, Zhang Q Y, Zhao J, Hao Y J. 2015. Conserved vacuolar H⁺-ATPase subunit B1 improves salt stress tolerance in apple calli and tomato plants. Scientia Horticulturae, 197:107-116. doi: 10.1016/j.scienta.2015.09.019 URL
[34]	Hussain S B, Shi C Y, Guo L X, Du W, Bai Y X, Kamran H M, Fernie A R, Liu Y Z. 2020. Type I H⁺-pyrophosphatase regulates the vacuolar storage of sucrose in citrus fruit. Journal of Experimental Botany, 71 (19):5935-5947. doi: 10.1093/jxb/eraa298 pmid: 32589717
[35]	Hussain S B, Shi C Y, Guo L X, Kamran H M, Sadka A, Liu Y Z. 2017. Recent advances in the regulation of citric acid metabolism in citrus fruit. Critical Reviews in Plant Sciences, 36 (4):241-256. doi: 10.1080/07352689.2017.1402850 URL
[36]	Janicka-Russak M, Kłobus G. 2007. Modification of plasma membrane and vacuolar H⁺-ATPases in response to NaCl and ABA. Journal of Plant Physiology, 164 (3):295-302. doi: 10.1016/j.jplph.2006.01.014 pmid: 16542749
[37]	Jia D, Wu P, Shen F, Li W, Zheng X, Wang Y, Yuan Y, Zhang X, Han Z. 2021. Genetic variation in the promoter of an R2R3-MYB transcription factor determines fruit malate content in apple(Malus domestica Borkh.). Plant Physiology, 186 (1):549-568. doi: 10.1093/plphys/kiab098 URL
[38]	Kabala K, Janicka-Russak M, Reda M, Migocka M. 2014. Transcriptional regulation of the V-ATPase subunit c and V-PPase isoforms in Cucumis sativus under heavy metal stress. Physiologia Plantarum, 150 (1):32-45. doi: 10.1111/ppl.12064 URL
[39]	Krebs M, Beyhl D, Gorlich E, Al-Rasheid K A, Marten I, Stierhof Y D, Hedrich R, Schumacher K. 2010. Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proceedings of the National Academy of Sciences of the United States of America, 107 (7):3251-3256.
[40]	Kriegel A, Andres Z, Medzihradszky A, Kruger F, Scholl S, Delang S, Patir-Nebioglu M G, Gute G, Yang H, Murphy A S, Peer W A, Pfeiffer A, Krebs M, Lohmann J U, Schumacher K. 2015. Job sharing in the endomembrane system:vacuolar acidification requires the combined activity of V-ATPase and V-PPase. Plant Cell, 27 (12):3383-3396. doi: 10.1105/tpc.15.00733 URL
[41]	Ladaniya M S. 2008. Citrus fruit:biology,technology and evaluation. Elsevier,135-137.
[42]	Li Da-pei, Wang Yi, Zhang Shang-kun, Zhao Xiang, Zhao Huan-yuan, Liu Yu-mei, Yang Gui-yan. 2019. Drought resistance analysis of a V- ATPase c subunit(JrVHAc4)gene from Juglans regia. Journal of Nanjing Forestry University(Natural Sciences Edition), 43 (2):79-85. (in Chinese)
	李大培, 王艺, 张尚昆, 赵翔, 赵焕元, 刘玉梅, 杨桂燕. 2019. 核桃 V-ATPase c 亚基基因(Jr VHAc4)的克隆和抗旱功能分析. 南京林业大学学报(自然科学版), 43 (2):79-85.
[43]	Li S J, Yin X R, Xie X L, Allan A C, Ge H, Shen S L, Chen K S. 2016a. The citrus transcription factor,CitERF13,regulates citric acid accumulation via a protein-protein interaction with the vacuolar proton pump,CitVHA-c4. Scientific Reports,620151.
[44]	Li Y, Provenzano S, Bliek M, Spelt C, Appelhagen I, Machado de Faria L, Verweij W, Schubert A, Sagasser M, Seidel T, Weisshaar B, Koes R, Quattrocchio F. 2016b. Evolution of tonoplast P-ATPase transporters involved in vacuolar acidification. New Phytologist, 211 (3):1092-1107. doi: 10.1111/nph.14008 URL
[45]	Liang Gui-hong, Hua Ying-peng, Zhou Ting, Song Hai-xing, Zhang Zhen-hua. 2020. Research progress on plant vacuolar membrane H⁺-ATPase and H⁺-PPase. Journal of Agricultural Science and Technology, 22 (1):19-27. (in Chinese)
	梁桂红, 华营鹏, 周婷, 宋海星, 张振华. 2020. 植物液泡膜H⁺-ATPase和H⁺-PPase 研究进展. 中国农业科技导报, 22 (1):19-27. doi: 10.13304/j.nykjdb.2018.0792
[46]	Lin S M, Tsai J Y, Hsiao C D, Huang Y T, Chiu C L, Liu M H, Tung J Y, Liu T H, Pan R L, Sun Y J. 2012. Crystal structure of a membrane-embedded H⁺-translocating pyrophosphatase. Nature, 484 (7394):399-403. doi: 10.1038/nature10963 URL
[47]	Liu Y, Zhang J, Liu H, Huang W. 2008. Salicylic acid or heat acclimation pre-treatment enhances the plasma membrane-associated ATPase activities in young grape plants under heat shock. Scientia Horticulturae, 119(1),21-27. doi: 10.1016/j.scienta.2008.06.027 URL
[48]	Ma B, Gao M, Zhang L, Zhao H, Zhu L, Su J, Li C, Li M, Ma F, Yuan Y. 2020. Genome-wide identification and characterization of apple P_3A-type ATPase genes,with implications for alkaline stress responses. Forests, 11 (3):292. doi: 10.3390/f11030292 URL
[49]	Ma B Q, Liao L, Fang T, Peng Q, Ogutu C, Zhou H, Ma F W, Han Y P. 2019. A Ma 10 gene encoding P-type ATPase is involved in fruit organic acid accumulation in apple. Plant Biotechnology Journal, 17 (3):674-686. doi: 10.1111/pbi.13007 URL
[50]	Maeshima M. 2000. Vacuolar H⁺-pyrophosphatase. Biochimica et Biophysica Acta-Biomembranes, 1465 (1-2):37-51. doi: 10.1016/S0005-2736(00)00130-9 URL
[51]	Martinoia E, Maeshima M, Neuhaus H E. 2007. Vacuolar transporters and their essential role in plant metabolism. Journal of Experimental Botany, 58 (1):83-102. doi: 10.1093/jxb/erl183 pmid: 17110589
[52]	Maruyama C, Tanaka Y, Takeyasu K, Yoshida M, Sato M H. 1998. Structural studies of the vacuolar H⁺-pyrophosphatase:sequence analysis and identification of the residues modified by fluorescent cyclohexylcarbodiimide and maleimide. Plant and cell physiology, 39 (10):1045-1053. pmid: 9871364
[53]	Michelet B, Boutry M. 1995. The plasma membrane H⁺-ATPase(a highly regulated enzyme with multiple physiological functions). Plant Physiology, 108 (1):1-6. doi: 10.1104/pp.108.1.1 pmid: 12228449
[54]	Milner I D, Ho L C, Hall J L. 1995. Properties of proton and sugar transport at the tonoplast of tomato(Lycopersicon esculentum)fruit. Physiologia Plantarum, 94 (3):399-410. doi: 10.1111/j.1399-3054.1995.tb00945.x URL
[55]	Mohammed S A, Nishio S, Takahashi H, Shiratake K, Ikeda H, Kanahama K, Kanayama Y. 2012. Role of vacuolar H⁺-inorganic pyrophosphatase in tomato fruit development. Journal of experimental botany, 63 (15),5613-5621. doi: 10.1093/jxb/ers213 pmid: 22915738
[56]	Müller M L, Taiz L. 2002. Regulation of the lemon-fruit V-ATPase by variable stoichometry and organic acids. Journal of Membrane Biology, 185:209-220. pmid: 11891579
[57]	Müller M, Irkens-Kiesecker U, Rubinstein B, Taiz L. 1996. On the mechanism of hyperacidification in lemon. Comparison of the vacuolar H⁺-ATPase activities of fruits and epicotyls. Journal of Biological Chemistry, 271 (4):1916-1924. doi: 10.1074/jbc.271.4.1916 pmid: 8567639
[58]	Nakanishi Y, Maeshima M. 1998. Molecular cloning of vacuolar H⁺-pyrophosphatase and its developmental expression in growing hypocotyl of mung bean. Plant Physiology, 116 (2):589-597. pmid: 9489011
[59]	Nelson H, Mandiyan S, Nelson N. 1989. A conserved gene encoding the 57-kDa subunit of the yeast vacuolar H⁺-ATPase. Journal of Biological Chemistry, 264 (3):1775-1778. pmid: 2521486
[60]	Park S, Li J, Pittman J K, Berkowitz G A, Yang H, Undurraga S, Morris J, Hirschi K D, Gaxiola R A. 2005. Up-regulation of a H⁺-pyrophosphatase (H⁺-PPase)as a strategy to engineer drought-resistant crop plants. Proceedings of the National Academy of Sciences of the United States of America, 102 (52):18830-18835.
[61]	Pedersen C N, Axelsen K B, Harper J F, Palmgren M G. 2012. Evolution of plant P-type ATPases. Frontiers in Plant Science, 3:31. doi: 10.3389/fpls.2012.00031 pmid: 22629273
[62]	Pedersen P L, Carafoli E. 1987. Ion motive ATPases. Ⅰ. Obiquity,properties,and significance to cell function. Trends in Biochemical Sciences, 12:146-150. doi: 10.1016/0968-0004(87)90071-5 URL
[63]	Portillo F. 2000. Regulation of plasma membrane H⁺-ATPase in fungi and plants. Biochimica et Biophysica Acta, 1469 (1):31-42. doi: 10.1016/s0304-4157(99)00011-8 pmid: 10692636
[64]	Schumacher K, Krebs M. 2010. The V-ATPase:small cargo,large effects. Current Opinion in Plant Biology, 13 (6):724-730. doi: 10.1016/j.pbi.2010.07.003 pmid: 20801076
[65]	Segami S, Nakanishi Y, Sato M H, Maeshima M. 2010. Quantification,organ-specific accumulation and intracellular localization of type Ⅱ H⁺-pyrophosphatase in Arabidopsis thaliana. Plant and Cell Physiology, 51 (8):1350-1360. doi: 10.1093/pcp/pcq096 pmid: 20605924
[66]	Shi C Y, Hussain S B, Guo L X, Yang H, Ning D Y, Liu Y Z. 2018. Genome-wide identification and transcript analysis of vacuolar-ATPase genes in citrus reveal their possible involvement in citrate accumulation. Phytochemistry, 155:147-154. doi: 10.1016/j.phytochem.2018.08.007 URL
[67]	Shi C Y, Hussain S B, Yang H, Bai Y X, Khan M A, Liu Y Z. 2019. CsPH8,a P-type proton pump gene,plays a key role in the diversity of citric acid accumulation in citrus fruits. Plant Science,289110288.
[68]	Shi C Y, Hussain S B, Han H, Alam S M, Liu D, Liu Y Z. 2021. Reduced expression of CsPH8,a P-type ATPase gene,is the major factor leading to the low citrate accumulation in citrus leaves. Plant Physiology and Biochemistry, 160:211-217. doi: 10.1016/j.plaphy.2021.01.019 URL
[69]	Shi C Y, Song R Q, Hu X M, Liu X, Jin L F, Liu Y Z. 2015. Citrus PH5-like H⁺-ATPase genes:identification and transcript analysis to investigate their possible relationship with citrate accumulation in fruits. Frontiers in Plant Science,6135.
[70]	Shiratake K, Kanayama Y, Maeshima M, Yamaki S. 1997. Changes in H⁺-pumps and a tonoplast intrinsic protein of vacuolar membranes during the development of pear fruit. Plant and Cell Physiology, 38 (9):1039-1045. pmid: 9360322
[71]	Strazzer P, Spelt C E, Li S, Bliek M, Federici C T, Roose M L, Koes R, Quattrocchio F M. 2019. Hyperacidification of Citrus fruits by a vacuolar proton-pumping P-ATPase complex. Nature Communacation, 10 (1):744.
[72]	Suzuki Y, Kanayama Y, Shiratake K, Yamaki S. 1999. Vacuolar H⁺-pyrophosphatase puri^®ed from pear fruit. Phytochemistry, 50:535-539. pmid: 10028695
[73]	Sze H, Schumacher K, Muller M L, Padmanaban S, Taiz L. 2002. A simple nomenclature for a complex proton pump:VHA genes encode the vacuolar H⁺-ATPase. Trends in Plant Science, 7 (4):157-161. doi: 10.1016/S1360-1385(02)02240-9 URL
[74]	Takanokura Y, Komatsu A, Omura M, Akihama T. 1998. Cloning and expression analysis of vacuolar H⁺-ATPase 69-kDa catalytic subunit cDNA in citrus(Citrus unshiu Marc.). Biochimica et Biophysica Acta-Biomembranes, 1414 (1-2):265-272. doi: 10.1016/S0005-2736(98)00148-5 URL
[75]	Terrier N, Deguilloux C, Sauvage F X, Martinoia E, Romieu C. 1998. Proton pumps and anion transport in Vitis vinifera:the inorganic pyrophosphatase plays a predominant role in the energization of the tonoplast. Plant Physiology and Biochemistry, 36 (5):367-377. doi: 10.1016/S0981-9428(98)80078-8 URL
[76]	Terrier N, Sauvage F X, Ageorges A, Romieu C. 2001. Changes in acidity and in proton transport at the tonoplast of grape berries during development. Planta, 213:20-28. pmid: 11523652
[77]	Tsiantis M S, Bartholomew D M, Smith J A C. 1996. Salt regulation of transcript levels for the c subunit of a leaf vacuolar H⁺-ATPase in the halophyte Mesembryanthemum crystallinum. The Plant Journal, 9(5):729-736. doi: 10.1046/j.1365-313X.1996.9050729.x URL
[78]	Venter M, Groenewald J H, Botha F C. 2006. Sequence analysis and transcriptional profiling of two vacuolar H⁺-pyrophosphatase isoforms in Vitis vinifera. Journal of Plant Research, 119 (5):469-478. doi: 10.1007/s10265-006-0009-4 URL
[79]	Verweij W, Spelt C, Di Sansebastiano G P, Vermeer J, Reale L, Ferranti F, Koes R, Quattrocchio F. 2008. An H⁺ P-ATPase on the tonoplast determines vacuolar pH and flower colour. Nature Cell Biology, 10 (12):1456-1462. doi: 10.1038/ncb1805 pmid: 18997787
[80]	Verweij W, Spelt C E, Bliek M, de Vries M, Wit N, Faraco M, Koes R, Quattrocchio F M. 2016. Functionally similar WRKY proteins regulate vacuolar acidification in petunia and hair development in Arabidopsis. Plant Cell, 28 (3):786-803. doi: 10.1105/tpc.15.00608 URL
[81]	Wang Bei-bei, Zhang Le, Guo Huan, Bao Ai-ke. 2020. Research progress on plant H⁺-PPase. Plant Physiology Journal, 56 (6):1109-1118. (in Chinese)
	王贝贝, 张乐, 郭欢, 包爱科. 2020. 植物H⁺-PPase研究进展. 植物生理学报, 56 (6):1109-1118.
[82]	Wang T, Li J, Guo S R, Gao H B, Wang S P. 2005. Effects of exogenous polyamines on the growth and activities of H⁺-ATPase and H⁺-PPase in cucumber seedling roots under hypoxia stress. Journal of Plant Physiology and Molecular Biology, 31 (6):637-642.
[83]	Wang J G, Zhou A M, Li Y, Li S S, Zhang X H, Che D D. 2016. Overexpression of IrlVHA-c,a vacuolar-type H⁺-ATPase c subunit gene from Iris lactea,enhances salt tolerance in tobacco. Plant Molecular Biology Reporter, 34 (5):877-885. doi: 10.1007/s11105-015-0969-4 URL
[84]	Wdowikowska A, Klobus G. 2016. The plasma membrane proton pump gene family in cucumber. Acta Physiologiae Plantarum, 38 (6):135. doi: 10.1007/s11738-016-2152-4 URL
[85]	Xu Z, Zhao Y, Ge Y, Peng J, Dong M, Yang G. 2017. Characterization of a vacuolar H⁺-ATPase G subunit gene from Juglans regia(JrVHAG1)involved in mannitol-induced osmotic stress tolerance. Plant Cell Reports, 36 (3):407-418. doi: 10.1007/s00299-016-2090-z URL
[86]	Yang J, Zhang J, Niu X Q, Zheng X L, Chen X, Zheng G H, Wu J C. 2021. Comparative transcriptome analysis reveals key genes potentially related to organic acid and sugar accumulation in loquat. PLoS ONE, 16 (4):e0238873. doi: 10.1371/journal.pone.0238873 URL
[87]	Yang L T, Xie C Y, Jiang H X, Chen L S. 2011. Expression of six malate-related genes in pulp during the fruit development of two loquat (Eriobotrya japonica)cultivars differing in fruit acidity. African Journal of Biotechnology, 10 (13):2414-2422.
[88]	Yao Y X, Dong Q L, You C X, Zhai H, Hao Y J. 2011. Expression analysis and functional characterization of apple MdVHP1 gene reveals its involvement in Na⁺,malate and soluble sugar accumulation. Plant Physiology and Biochemistry, 49 (10):1201-1208. doi: 10.1016/j.plaphy.2011.05.012 URL
[89]	Yoshida K, Kawachi M, Mori M, Maeshima M, Kondo M, Nishimura M, Kondo T. 2005. The involvement of tonoplast proton pumps and Na⁺ (K⁺)/H⁺ exchangers in the change of petal color during flower opening of morning glory,Ipomoea tricolor cv. Heavenly Blue. Plant and Cell Physiology, 46 (3):407-415. pmid: 15695444
[90]	Zhang C M, Hao Y J. 2020. Advances in genomic,transcriptomic,and metabolomic analyses of fruit quality in fruit crops. Horticultural Plant Journal, 6 (6):361-371. doi: 10.1016/j.hpj.2020.11.001 URL
[91]	Zhang Y, Li Q, Xu L, Qiao X, Liu C, Zhang S. 2020. Comparative analysis of the P-type ATPase gene family in seven Rosaceae species and an expression analysis in pear(Pyrus bretschneideri Rehd.). Genomics, 112 (3):2550-2563. doi: 10.1016/j.ygeno.2020.02.008 URL
[92]	Zhou H, Huang W, Luo S, Hu H, Zhang Y, Zhang L, Li P. 2020. Genome-wide identification of the vacuolar H⁺-ATPase gene family in five rosaceae species and expression analysis in pear(Pyrus bretschneideri). Plants (Basel), 9 (12):1661.
[93]	Zheng B B, Zhao L, Jiang X H, Cherono S, Liu J J, Ogutu C, Ntini C, Zhang X J, Han Y P. 2021. Assessment of organic acid accumulation and its related genes in peach. Food Chemistry, 334:127567. doi: 10.1016/j.foodchem.2020.127567 URL
[94]	Zhou Si-jie, Zhang Min, Wang Ping. 2021. Response of plant plasma membrane H⁺-ATPase to environmental stress factors:a review. China Journal of Applied and Environmental Biology, 27 (2):485-494.
	周思婕, 张敏, 王平. 2021. 植物质膜H⁺-ATP酶对环境胁迫因子的响应研究进展. 应用与环境生物学报, 27 (2):485-494.

园艺作物 Horticultural crop	基因数或活性 Gene number or enzyme activity			参考文献Reference
园艺作物 Horticultural crop	PHA	VHA	VHP	参考文献Reference
柑橘Citrus	8	20	3	Shi et al.，2015，2018;Hussain et al.，2020
苹果Apple	15	48	1	Yao et al.，2011;Dong et al.，2013;Hu et al.，2015;Ma et al.，2020;Zhou et al.，2020
梨Pear	11 ~ 16	43	活性Activity	Suzuki et al.，1999;Amemiya，2005;Zhang et al.，2020;Zhou et al.，2020
桃Peach	9	23	2	Etienne et al.，2002a;Zhang et al.，2020;Zhou et al.，2020
李Plum	0	25	0	Zhou et al.，2020
杏Apricot	9	0	0	Zhang et al.，2020
葡萄Grape	活性Activity	活性Activity	2	Terrier et al.，2001;Venter et al.，2006;Liu et al.，2008
枇杷Loquat	0	2	1	Yang et al.，2011，2021;李大培等，2019
核桃Walnut	0	1	0	Xu et al.，2017
草莓Strawberry	7	20	0	Zhang et al.，2020;Zhou et al.，2020
番茄Tomato	7/8	23	3	Ewing & Bennett，1994;Coker et al.，2003;Mohammed et al.，2012;
黄瓜Cucumber	10	2	1	Kaba?a et al.，2014;Wdowikowska & Klobus，2016
南瓜Pumpkin	0	0	1	Maruyama et al.，1998
番木瓜Papaya	活性Activity	0	0	Azevedo et al.，2008
矮牵牛Petunia	2	0	0	Veiweij et al.，2008;Faraco et al.，2014
白花马蔺White flower iris	0	1	0	Wang et al.，2016
冰叶日中花Ice plant	0	1	0	Tsiantis et al.，1996

园艺作物 Horticultural crop	基因数或活性 Gene number or enzyme activity			参考文献Reference
园艺作物 Horticultural crop	PHA	VHA	VHP	参考文献Reference
柑橘Citrus	8	20	3	Shi et al.，2015，2018;Hussain et al.，2020
苹果Apple	15	48	1	Yao et al.，2011;Dong et al.，2013;Hu et al.，2015;Ma et al.，2020;Zhou et al.，2020
梨Pear	11 ~ 16	43	活性Activity	Suzuki et al.，1999;Amemiya，2005;Zhang et al.，2020;Zhou et al.，2020
桃Peach	9	23	2	Etienne et al.，2002a;Zhang et al.，2020;Zhou et al.，2020
李Plum	0	25	0	Zhou et al.，2020
杏Apricot	9	0	0	Zhang et al.，2020
葡萄Grape	活性Activity	活性Activity	2	Terrier et al.，2001;Venter et al.，2006;Liu et al.，2008
枇杷Loquat	0	2	1	Yang et al.，2011，2021;李大培等，2019
核桃Walnut	0	1	0	Xu et al.，2017
草莓Strawberry	7	20	0	Zhang et al.，2020;Zhou et al.，2020
番茄Tomato	7/8	23	3	Ewing & Bennett，1994;Coker et al.，2003;Mohammed et al.，2012;
黄瓜Cucumber	10	2	1	Kaba?a et al.，2014;Wdowikowska & Klobus，2016
南瓜Pumpkin	0	0	1	Maruyama et al.，1998
番木瓜Papaya	活性Activity	0	0	Azevedo et al.，2008
矮牵牛Petunia	2	0	0	Veiweij et al.，2008;Faraco et al.，2014
白花马蔺White flower iris	0	1	0	Wang et al.，2016
冰叶日中花Ice plant	0	1	0	Tsiantis et al.，1996

Research Progress of Proton Pumps and Their Regulation in Organic Acid Accumulation in Horticultural Plants

RichHTML

PDF

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 2

References 94

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	YANG Zhi, ZHANG Chuanjiang, YANG Xinfang, DONG Mengyi, WANG Zhenlei, YAN Fenfen, WU Cuiyun, WANG Jiurui, LIU Mengjun, LIN Minjuan. Analysis of Fruit Genetic Tendency and Mixed Inheritance in Hybrid Progeny of Jujube and Wild Jujube [J]. Acta Horticulturae Sinica, 2023, 50(1): 36-52.
[2]	YUAN Xin, XU Yunhe, ZHANG Yupei, SHAN Nan, CHEN Chuying, WAN Chunpeng, KAI Wenbin, ZHAI Xiawan, CHEN Jinyin, GAN Zengyu. Studies on AcAREB1 Regulating the Expression of AcGH3.1 During Postharvest Ripening of Kiwifruit [J]. Acta Horticulturae Sinica, 2023, 50(1): 53-64.
[3]	SHAO Fengqing, LUO Xiurong, WANG Qi, ZHANG Xianzhi, WANG Wencai. Advances in Research of DNA Methylation Regulation During Fruit Ripening [J]. Acta Horticulturae Sinica, 2023, 50(1): 197-208.
[4]	WANG Yingying, LIU Lichang, LIU Zhiwu, YANG Xingwang, LIU Wanchun, and WANG Xiaodi, . A New Little Nectarine Cultivar‘Zhongnong Zhenzhu’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 25-26.
[5]	SONG Fang, CHEN Qi, YUAN Yanliang, CHEN Sha, YIN Haijun, and JIANG Yingchun, . A New Yellow-fleshed Kiwifruit Cultivar‘Xianwo 1’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 47-48.
[6]	QI Yongjie, GAO Zhenghui, MA Na, WANG Qingming, KE Fanjun, CHEN Qian, and XU Yiliu, . A New Yellow Flesh and Resistant to Canker Disease Kiwifruit Cultivar ‘Wannong Jinguo’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 49-50.
[7]	ZHANG Huiqin, LOU Guorong, LU Linghong, GU Xianbin, SONG Genhua, and XIE Ming. A New Yellow-fleshed Kiwifruit Cultivar‘Jinyi’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 51-52.
[8]	Patiguli Maimaitituerxun, Gulinisha Kasimu, LUO Qinghong, LIU Liyan, LIU Qiaoling, and Reyihan Awutitashi. A New Cultivar of Elaeagnus moorcroftii‘Yafeng’in Xinjiang [J]. Acta Horticulturae Sinica, 2022, 49(S2): 69-70.
[9]	ZHAO Xia, LI Gang, LIU Lifeng, SONG Yanhong, and ZHOU Houcheng. A New Strawberry Cultivar‘Huashuo 1’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 81-82.
[10]	LI Zhengli, ZHANG Li, and MA Licang. A New Capsicum frutescens Cultivar‘Huangla Chaotian’with Yellow Fruit [J]. Acta Horticulturae Sinica, 2022, 49(S2): 123-124.
[11]	GAO Zhihong, NI Zhaojun, SHI Ting, HAN Jian, and ZHANG Zhen. A Novel Cultivar of Prunus mume‘Nannong Fengyu’for Ornamental Value and Fruit Production [J]. Acta Horticulturae Sinica, 2022, 49(S2): 259-260.
[12]	LU Lu, LI Wenqing, WU Dan, WANG Zhen, LIU Li, WANG Lei, XIE Xiaoman, and ZHAO Yongjun, . A New Xanthoceras sorbifolium Cultivar‘Xiaozhenzhu’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 275-276.
[13]	QIN Gaihua, LIU Chunyan, LI Jiyu, and XU Yiliu, . A New Pomegranate Cultivar‘Suzi’ [J]. Acta Horticulturae Sinica, 2022, 49(S1): 39-40.
[14]	WANG Yan, LIU Zhenshan, ZHANG Jing, YANG Pengfei, MA Lan, WANG Zhiyi, TU Hongxia, YANG Shaofeng, WANG Hao, CHEN Tao, WANG Xiaorong. Inheritance Trend of Flower and Fruit Traits in F₁ Progenies of Chinese Cherry [J]. Acta Horticulturae Sinica, 2022, 49(9): 1853-1865.
[15]	MENG Xiaoyu, MU Yue, HU Yang, WU Xiao, ZHU Chen, WANG Huimin, TAO Shutian, ZHANG Shaoling, YIN Hao. Determination of Fruit Surface Area of Several Fruit by 3D Laser Scanning Technology [J]. Acta Horticulturae Sinica, 2022, 49(9): 1998-2006.