Please wait a minute...
Journal of Integrative Agriculture  2026, Vol. 25 Issue (9): 3572-3584    DOI: 10.1016/j.jia.2024.12.031
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide characterization of soybean lysophosphatidic acid acyltransferases and functional characterization of the role of GmLPAT11 in salt stress

Zhiyang Wang*, Peiyan Liu*, Haitong Sun, Wenying Suo, Ziqian Cheng, Mingliang Yang#, Qingshan Chen#, Ying Zhao#

National Key Laboratory of Smart Farm Technology and Systems/Key Laboratory of Soybean Biology, Ministry of Education/Northeast Agricultural University, Harbin 150030, China 

 Highlights 

Under salt stress, GmLPAT11 enhances soybean salt tolerance by regulating antioxidant activity and redox status.

Two haplotypes of the GmLPAT11 gene were identified.  The natural variation of GmLPAT11 is crucial for its function, with Hap2 being a favorable haplotype for salt tolerance.

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

溶血磷脂酸酰基转移酶(LPAT)是一种广泛表达的酶,在植物的生长发育和胁迫响应中起着关键作用。然而,关于大豆基因组中的LPAT基因的信息却十分有限。通过全基因组分析,鉴定了15个大豆LPAT家族成员,并分析了保守蛋白基序的存在。根据其系统发育关系,将这些基因分为三个聚类。通过共聚焦显微镜在拟南芥叶肉原生质体上测定了6GmLPATs的胞内定位。顺式调节元件分析和实时定量聚合酶链反应(qRT-PCR)的结果显示,非生物胁迫(干旱、盐和碱度)和激素处理显著增加了GmLPATs的转录本。GmLPATs在不同的大豆组织中表现出独特的表达模式。我们发现,一个soiLPAT亚型GmLPAT11)在各个处理下的表达水平较高,这可能表明它在大豆对盐胁迫的响应中起了关键作用。GmLPAT11在大肠杆菌中的表达表明,重组酶具有LPAT活性。我们还发现过表达LPAT降低了转基因大豆活性氧(ROS)的形成,显著提高了抗盐胁迫性。基因关联分析表明,GmLPAT11的变异与幼苗的耐盐性密切相关。在GmLPAT11CDS区发现了一种可能与耐盐性相关的多态性。这些发现不仅提高了我们对LPAT基因家族的理解,还确定了大豆未来增强耐盐性的潜在候选基因。



Abstract  

Lysophosphatidic acid acyltransferase (LPAT) enzymes are widely expressed in various plant species, and they contribute to growth, development, and stress responses.  Currently,  information regarding the LPAT gene family in soybeans is limited.  In this study, genome-wide analyses identified 15 soybean LPATs, which were then evaluated for their conserved protein motifs.  These genes were grouped into three clusters based on their phylogenetic relationships.  Confocal microscopy was used to visualize the localization of six GmLPATs within Arabidopsis mesophyll protoplasts.  cis-Acting regulatory element analyses and qRT-PCR experiments revealed that these GmLPATs were upregulated in response to hormonal stimulation or exposure to abiotic stressors, including drought, alkaline conditions, and salt stress.  The expression patterns of these GmLPATs varied among different soybean tissue types.  One member of the solLPAT1 subtype (GmLPAT11) was found to be upregulated in response to a range of treatments, highlighting its role in soybean salt stress responses.  GmLPAT11 expression in Escherichia coli confirmed the LPAT activity of this recombinant enzyme, and overexpressing this LPAT reduced reactive oxygen species production in transgenic soybean plants, thereby enhancing their salt stress tolerance.  Gene association analyses indicated that GmLPAT11 variants are closely associated with seedling salt tolerance, and a polymorphism in the GmLPAT11 CDS region was potentially associated with salt tolerance.  These results provide new insights into the nature of the LPAT gene family in soybeans while also identifying promising candidate genes for future research efforts to enhance the overall salt tolerance of soybean crops. 

Keywords:  soybean (Glycine max (L.) Merr.)       Lysophosphatidic acid acyltransferase       salt stress       expression pattern  
Received: 20 September 2024   Accepted: 25 November 2024 Online: 28 December 2024  
Fund: 

This study was financially supported by the Natural Science Foundation of Heilongjiang Province, China (TD2022C003 and YQ2022C010), the National Key R&D Program of China (2023ZD040360305), and the National Natural Science Foundation of China (U20A2027, U23A201783, 32272093, and 32272072).

About author:  Zhiyang Wang, E-mail: wzy13613642168@163.com; Peiyan Liu, E-mail: liupeiyan823@163.com; #Correspondence Mingliang Yang, Tel: +86-451-55191945, E-mail: mlyang@neau.edu.cn; Qingshan Chen, Tel: +86-451-55191259, E-mail: qshchen@126.com; Ying Zhao, E-mail: tianshi198937@126.com * These authors contributed equally to this study.

Cite this article: 

Zhiyang Wang, Peiyan Liu, Haitong Sun, Wenying Suo, Ziqian Cheng, Mingliang Yang, Qingshan Chen, Ying Zhao. 2026. Genome-wide characterization of soybean lysophosphatidic acid acyltransferases and functional characterization of the role of GmLPAT11 in salt stress. Journal of Integrative Agriculture, 25(9): 3572-3584.

Ali U, Lu S, Fadlalla T, Iqbal S, Yue H, Yang B, Hong Y, Wang X, Guo L. 2022. The functions of phospholipases and their hydrolysis products in plant growth, development and stress responses. Progress in Lipid Research86, 101158.

Angkawijaya A E, Nguyen V C, Nakamura Y. 2017. Enhanced root growth in phosphate-starved Arabidopsis by stimulating de novo phospholipid biosynthesis through the overexpression of LYSOPHOSPHATIDIC ACID ACYLTRANSFERASE 2 (LPAT2). Plant Cell and Environment40, 1807–1818.

Arroyo-Caro J M, Chileh T, Kazachkov M, Zou J, Alonso D L, García-Maroto F. 2013. The multigene family of lysophosphatidate acyltransferase (LPAT)-related enzymes in Ricinus communis: Cloning and molecular characterization of two LPAT genes that are expressed in castor seeds. Plant Science199–200, 29–40.

Bargmann B O R, Laxalt A M, Riet B T, van Schooten B, Merquiol E, Testerink C, Haring M A, Bartels D, Munnik T. 2008. Multiple PLDs required for high salinity and water deficit tolerance in plants. Plant and Cell Physiology50, 78–89.

Bourgis F, Kader J C, Barret P, Renard M, Robinson D, Robinson C, Delseny M, Roscoe T J. 1999. A plastidial lysophosphatidic acid acyltransferase from oilseed rape. Plant Physiology120, 913–922.

Brown A P, Coleman J, Tommey A M, Watson M D, Slabas A R. 1994. Isolation and characterisation of a maize cDNA that complements a 1-acyl sn-glycerol-3-phosphate acyltransferase mutant of Escherichia coli and encodes a protein which has similarities to other acyltransferases. Plant Molecular Biology26, 211–223.

Bustin S A, Benes V, Garson J A, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl M W, Shipley G L, Vandesompele J, Wittwer C T. 2009. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry55, 611–622.

Chapman K D, Ohlrogge J B. 2012. Compartmentation of triacylglycerol accumulation in plants. Journal of Biological Chemistry, 287, 2288–2294.

Chen J, Zhang P, Zhao Y, Zhao J, Wu X, Zhang R, Cha R, Yao Q, Gao Y. 2022. Nitroreductase-instructed supramolecular assemblies for microbiome regulation to enhance colorectal cancer treatments. Science Advances8, eadd2789.

Chen S L, Huang J Q, Lei Y, Zhang Y T, Ren X P, Chen Y N, Jiang H F, Yan L Y, Li Y R, Liao B S. 2012. Identification and characterization of a gene encoding a putative lysophosphatidyl acyltransferase from Arachis hypogaeaJournal of Bioscience and Bioengineering37, 1029–1039.

Chen X, Wang Y, Wang J N, Cao Q C, Sun R X, Zhu H J, Zhang Y R, Ji J D, Liu Q H. 2022. m6A modification of circSPECC1 suppresses RPE oxidative damage and maintains retinal homeostasis. Cell Reports41, 111671.

Chen Y, Fu Z, Zhang H, Tian R, Yang H, Sun C, Wang L, Zhang W, Guo Z, Zhang X, Tang J. 2020. Cytosolic malate dehydrogenase 4 modulates cellular energetics and storage reserve accumulation in maize endosperm. Plant Biotechnology Journal18, 2420–2435.

Dai H F Wu H, Amanguli Maimaiti Ali A, Wang L H, Apizi M, Zhang J S. 2014. Analysis of salt-tolerance and determination of salt-tolerant evaluation indicators in cotton seedlings of different genotypes. Scientia Agricultura Sinica, 47, 1290–1300. (in Chinese)

Fryer M J, Oxborough K, Mullineaux P M, Baker N R. 2002. Imaging of photo-oxidative stress responses in leaves. Journal of Experimental Botany53, 1249–1254.

Giannopolitis C N, Ries S K. 1977. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology59, 309–314.

Han R H, Lu X S, Gao G J, Yang X J. 2006. Analysis of the principal components and the subordinate function of alfalfa drought resistance. Acta Agrestia Sinica14, 142–146. (in Chinese)

Hanke C, Wolter F P, Coleman J, Peterek G, Frentzen M. 1995. A plant acyltransferase involved in triacylglycerol biosynthesis complements an Escherichia coli sn-1-acylglycerol-3-phosphate acyltransferase mutant. European Journal of Biochemistry232, 806–810.

Hasegawa P M. 2013. Sodium (Na+) homeostasis and salt tolerance of plants. Environmental and Experimental Botany92, 19–31.

Hong Y, Pan X, Welti R, Wang X. 2008. Phospholipase Dα3 is involved in the hyperosmotic response in ArabidopsisThe Plant Cell20, 803–816.

Hong Y, Zhao J, Guo L, Kim S C, Deng X, Wang G, Zhang G, Li M, Wang X. 2016. Plant phospholipases D and C and their diverse functions in stress responses. Progress in Lipid Research62, 55–74.

Hossain M S, Dietz K J. 2016. Tuning of redox regulatory mechanisms, reactive oxygen species and redox homeostasis under salinity stress. Frontiers in Plant Science7, 548.

Kim H U, Huang A H C. 2004. Plastid lysophosphatidyl acyltransferase is essential for embryo development in ArabidopsisPlant Physiology134, 1206–1216.

Kim H U, Li Y, Huang A H. 2005. Ubiquitous and endoplasmic reticulum-located lysophosphatidyl acyltransferase, LPAT2, is essential for female but not male gametophyte development in ArabidopsisPlant Cell17, 1073–1089.

Kim H U, Vijayan P, Carlsson A S, Barkan L, Browse J. 2010. A mutation in the LPAT1 gene suppresses the sensitivity of fab1 plants to low temperature. Plant Physiology153, 1135–1143.

Knutzon D S, Lardizabal K D, Nelsen J S, Bleibaum J L, Davies H M, Metz J G. 1995. Cloning of a coconut endosperm cDNA encoding a 1-acyl-sn-glycerol-3-phosphate acyltransferase that accepts medium-chain-length substrates. Plant Physiology109, 999–1006.

Kolkman J A, Stemmer W P. 2001. Directed evolution of proteins by exon shuffling. Nature Biotechnology19, 423–428.

Lewin T M, Wang P, Coleman R A. 1999. Analysis of amino acid motifs diagnostic for the sn-glycerol-3-phosphate acyltransferase reaction. Biochemistry38, 5764–5771.

Liu M, Wu S, Walch H, Grigoriev A. 2005. Exon-domain correlation and its corollaries. Bioinformatics21, 3213–3216.

Liu W, Xie Y, Ma J, Luo X, Nie P, Zuo Z, Lahrmann U, Zhao Q, Zheng Y, Zhao Y, Xue Y, Ren J. 2015. IBS: An illustrator for the presentation and visualization of biological sequences. Bioinformatics31, 3359–3361.

Maisonneuve S, Bessoule J J, Lessire R, Delseny M, Roscoe T J. 2010. Expression of rapeseed microsomal lysophosphatidic acid acyltransferase isozymes enhances seed oil content in ArabidopsisPlant Physiology152, 670–684.

Mishra G, Zhang W, Deng F, Zhao J, Wang X. 2006. A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in ArabidopsisScience312, 264–266.

Misra N, Panda P K, Parida B K. 2014. Genome-wide identification and evolutionary analysis of algal LPAT genes involved in TAG biosynthesis using bioinformatic approaches. Molecular Biology Reports41, 8319–8332.

Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology22, 867–880.

Ohlrogge J, Browse J. 1995. Lipid biosynthesis. The Plant Cell7, 957–970.

Pokotylo I, Kravets V, Martinec J, Ruelland E. 2018. The phosphatidic acid paradox: Too many actions for one molecule class? Lessons from plants. Progress in Lipid Research71, 43–53.

Ruelland E, Kravets V, Derevyanchuk M, Martinec J, Zachowski A, Pokotylo I. 2015. Role of phospholipid signalling in plant environmental responses. Environmental and Experimental Botany114, 129–143.

Shaikh A A, Alamin A, Jia C, Gong W, Deng X, Shen Q, Hong Y. 2022. The examination of the role of rice lysophosphatidic acid acyltransferase 2 in response to salt and drought stresses. International Journal of Molecular Sciences23, 9796.

Sivakumar D, Sivaraman T. 2011. In silico designing and screening of lead compounds to NS5-methyltransferase of dengue viruses. Journal of Medicinal Chemistry7, 655–662.

Snyder C L, Yurchenko O P, Siloto R M, Chen X, Liu Q, Mietkiewska E, Weselake R J. 2009. Acyltransferase action in the modification of seed oil biosynthesis. Nature Biotechnology26, 11–16.

Tambasco-Studart M, Titiz O, Raschle T, Forster G, Amrhein N, Fitzpatrick T B. 2005. Vitamin B6 biosynthesis in higher plants. Proceedings of the National Academy of Sciences of the United States of America102, 13687–13692.

Taylor D C, Francis T, Lozinsky S, Hoffman T L, Giblin M E, Marillia E F. 2010. Cloning and characterization of a constitutive lysophosphatidic acid acyltransferase 2 (LPAT2) gene from Tropaeolum majus L. The Open Plant Science Journal4, 7–17.

Tóth K, Batek J, Stacey G. 2016. Generation of soybean (Glycine max) transient transgenic roots. Current Protocols in Plant Biology1, 1–13.

Velikova V, Yordanov I, Edreva A. 2000. Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science151, 59–66.

Wang D, Yuan M, Zhuang Y, Xin X F, Qi G. 2024. DGK5-mediated phosphatidic acid homeostasis interplays with reactive oxygen species in plant immune signaling. Journal of Integrative Plant Biology66, 1263–1265.

Wang P, Shen L, Guo J, Jing W, Qu Y, Li W, Bi R, Xuan W, Zhang Q, Zhang W. 2019. Phosphatidic acid directly regulates PINOID-dependent phosphorylation and activation of the PIN-FORMED2 auxin efflux transporter in response to salt stress. The Plant Cell31, 250–271.

Wang Q J, Sun H, Dong Q L, Sun T Y, Jin Z X, Hao Y J, Yao Y X. 2016. The enhancement of tolerance to salt and cold stresses by modifying the redox state and salicylic acid content via the cytosolic malate dehydrogenase gene in transgenic apple plants. Plant Biotechnology Journal14, 1986–1997.

Wang X, Devaiah S P, Zhang W, Welti R. 2006. Signaling functions of phosphatidic acid. Progress in Lipid Research45, 250–278.

Yoo S D, Cho Y H, Sheen J. 2007. Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nature Protocols2, 1565–1572.

Yu C Y, Zhang H K, Wang N, Sun J, Dong Y X, Zhang X S, Gao X Q. 2021. Characterization of the ERP gene family in Arabidopsis thalianaPlant Signaling and Behavior16, 1913301.

Zhang Q, Lin F, Mao T, Nie J, Yan M, Yuan M, Zhang W. 2012. Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in ArabidopsisThe Plant Cell24, 4555–4576.

Zhang R, Hussain S, Wang Y, Liu Y, Li Q, Chen Y, Wei H, Gao P, Dai Q. 2021. Comprehensive evaluation of salt tolerance in rice (Oryza sativa L.) germplasm at the germination stage. Agronomy11, 1569.

Zhang W, Qin C, Zhao J, Wang X. 2004. Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proceedings of the National Academy of Sciences of the United States of America101, 9508–9513.

Zhao Y, Cao P, Cui Y, Liu D, Li J, Zhao Y, Yang S, Zhang B, Zhou R, Sun M, Guo X, Yang M, Xin D, Zhang Z, Li X, Lv C, Liu C, Qi Z, Xu J, Wu X, Chen Q. 2021. Enhanced production of seed oil with improved fatty acid composition by overexpressing NAD+-
dependent glycerol-3-phosphate dehydrogenase in soybean. Journal of Integrative Plant Biology63, 1036–1053.

Zhou R N, Wang S H, Liu P Y, Cui Y F, Hu Z B, Liu C Y, Zhang Z G, Yang M L, Li X, Wu X X, Chen Q S, Zhao Y. 2025. Genome-wide characterization of soybean malate dehydrogenase genes reveals a positive role for GmMDH2 in the salt stress response. Journal of Integrative Agriculture24, 2492–2510.

[1] Min Xiong, Chuxin Wang, Xinrui Liang, Jiawen Yu, Tingting Liu, Bin Peng, Xiaoxuan Du, Tingyu Yang, Gongneng Feng, Qiaoquan Liu, Qianfeng Li. Multi-omics approach reveals the contribution of brassinosteroids to salt tolerance for seed germination in rice[J]. >Journal of Integrative Agriculture, 2026, 25(6): 2288-2298.
[2] Qi Zhao, Mengjie Cui, Tengda Guo, Lei Shi, Feiyan Qi, Ziqi Sun, Pei Du, Hua Liu, Yu Zhang, Zheng Zheng, Bingyan Huang, Wenzhao Dong, Suoyi Han, Xinyou Zhang. Genome-wide characterization and expression analysis of the cultivated peanut AhPR10 gene family mediating resistance to Aspergillus flavus[J]. >Journal of Integrative Agriculture, 2026, 25(1): 56-67.
[3] Qing Li, Zhuangzhuang Sun, Zihan Jing, Xiao Wang, Chuan Zhong, Wenliang Wan, Maguje Masa Malko, Linfeng Xu, Zhaofeng Li, Qin Zhou, Jian Cai, Yingxin Zhong, Mei Huang, Dong Jiang. Time-course transcriptomic information reveals the mechanisms of improved drought tolerance by drought priming in wheat[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2902-2919.
[4] Ke Fang, Yi Liu, Zhiquan Wang, Xiang Zhang, Xuexiao Zou, Feng Liu, Zhongyi Wang. Genome-wide analysis of the CaYABBY family in pepper and functional identification of CaYABBY5 in the regulation of floral determinacy and fruit morphogenesis[J]. >Journal of Integrative Agriculture, 2025, 24(8): 3024-3039.
[5] Runnan Zhou, Sihui Wang, Peiyan Liu, Yifan Cui, Zhenbang Hu, Chunyan Liu, Zhanguo Zhang, Mingliang Yang, Xin Li, Xiaoxia Wu, Qingshan Chen, Ying Zhao. Genome-wide characterization of soybean malate dehydrogenase genes reveals a positive role for GmMDH2 in the salt stress response[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2492-2510.
[6] Zhian Dai, Rongwei Yuan, Xiangxia Yang, Hanxiao Xi, Ma Zhuo, Mi Wei. Salinity-responsive key endophytic bacteria in the propagules of Kandelia obovata enhance salt tolerance in rice[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1738-1753.
[7] Xiang Lu, Qian Zuo, Md. Nurul Huda, Yaliang Shi, Guangsheng Li, Xiangru Wang, Yawen Xiao, Muhammad Khurshid, Tanzim Jahan, Namraj Dhami, Dhurva Prasad Gauchan, Md. Arfan Ali, Jianping Cheng, Yu Meng, Jingjun Ruan, Meiliang Zhou. Genome-wide association analysis locates FtAUR3 in Tartary buckwheat that contributes to enhance plant salt resistance[J]. >Journal of Integrative Agriculture, 2025, 24(12): 4515-4527.
[8] Chang Liu, Lei Tian, Wenbo Yu, Yu Wang, Ziqing Yao, Yue Liu, Luomiao Yang, Chunjuan Liu, Xiaolong Shi, Tao Liu, Bingru Chen, Zhenguo Wang, Haiqiu Yu, Yufei Zhou. Natural variation in SbTEF1 contributes to salt tolerance in sorghum seedlings [J]. >Journal of Integrative Agriculture, 2025, 24(11): 4168-4181.
[9] Fuli Gao, Zidong Wang, Wankun Liu, Min Liu, Baoyi Wang, Yingjie Yang, Jiankun Song, Zhenhua Cui, Chenglin Liang, Dingli Li, Ran Wang, Jianlong Liu. Dehydrin PbDHN3 regulates ethylene synthesis and signal transduction to improve salt tolerance in pear[J]. >Journal of Integrative Agriculture, 2025, 24(10): 3838-3850.
[10] Congcong Zhang, Han Wang, Guojie Nai, Lei Ma, Xu Lu, Haokai Yan, Meishuang Gong, Yuanyuan Li, Ying Lai, Zhihui Pu, Li Wei, Guiping Chen, Ping Sun, Baihong Chen, Shaoying Ma, Sheng Li. Nitrogen application regulates antioxidant capacity and flavonoid metabolism, especially quercetin, in grape seedlings under salt stress[J]. >Journal of Integrative Agriculture, 2024, 23(12): 4074-4092.
[11] Caixiang Wang, Meili Li, Dingguo Zhang, Xueli Zhang, Juanjuan Liu, Junji Su. Knockdown of the atypical protein kinase genes GhABC1K2-A05 and GhABC1K12-A07 make cotton more sensitive to salt and PEG stress[J]. >Journal of Integrative Agriculture, 2024, 23(10): 3370-3386.
[12] MA Xiao-wen, MA Qiu-xiang, MA Mu-qing, CHEN Yan-hang, GU Jin-bao, LI Yang, HU Qing, LUO Qing-wen, WEN Ming-fu, ZHANG Peng, LI Cong, WANG Zhen-yu.

Cassava MeRS40 is required for the regulation of plant salt tolerance [J]. >Journal of Integrative Agriculture, 2023, 22(5): 1396-1411.

[13] LI Qiao-lu, LI Zhi-yong, WANG Meng-meng, YAN Jing-wei, FANG Lin. Phosphorylation of SiRAV1 at Ser31 regulates the SiCAT expression to enhance salt tolerance in Setaria italica[J]. >Journal of Integrative Agriculture, 2023, 22(12): 3638-3651.
[14] WANG Chu-kun, ZHAO Yu-wen, HAN Peng-liang, YU Jian-qiang, HAO Yu-jin, XU Qian, YOU Chun-xiang, HU Da-gang. Auxin response factor gene MdARF2 is involved in ABA signaling and salt stress response in apple[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2264-2274.
[15] LI Zhi-qi, Xie Qian, YAN Jia-hui, CHEN Jian-qing, CHEN Qing-xi. Genome-wide identification and characterization of the abiotic-stress-responsive lipoxygenase gene family in diploid woodland strawberry (Fragaria vesca)[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1982-1996.
No Suggested Reading articles found!