Please wait a minute...
Journal of Integrative Agriculture  2022, Vol. 21 Issue (7): 1982-1996    DOI: 10.1016/S2095-3119(21)63819-4
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide identification and characterization of the abiotic-stress-responsive lipoxygenase gene family in diploid woodland strawberry (Fragaria vesca)
LI Zhi-qi1, XIE Qian1, YAN Jiahui1,2, CHEN  Jian-qing1, CHEN Qing-xi1
1 College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, China
2 Horticulture Biology And Metabolomics Center, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou 350002, China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

本研究从二倍体森林草莓基因组中鉴定出14个LOX基因。系统发育树将FvLOX基因分为9-LOX和13-LOX两个亚家族。基因重复事件分析表明,全基因组复制/片段复制和分散复制有效地促进了草莓LOX家族的扩展。QRT-PCR分析表明,FvLOX基因在不同组织中均有不同程度的表达。表达谱分析表明,FvLOX1FvLOX8在低温胁迫下表达上调,FvLOX3FvLOX7在干旱胁迫下表达上调,FvLOX6FvLOX9在盐胁迫下表达上调,FvLOX2FvLOX3FvLOX6在SA处理下表达上调,FvLOX3FvLOX11FvLOX14在MeJA处理下表达上调,FvLOX4FvLOX14在ABA处理下表达上调。启动子分析表明,FvLOX基因参与植物生长发育和胁迫响应。我们对草莓FvLOX家族进行了全基因组分析和鉴定,表征了多种参与非生物胁迫响应的FvLOX候选基因,该研究为草莓在非生物胁迫中的响应机制奠定了理论和经验基础




Abstract  Lipoxygenase (LOXs) is a kind of dioxygenase without heme and iron, which plays an important role in the development and adaptation of many plants to the environment.  However, the study of strawberry LOX gene family has not been reported.  In this study, 14 LOX genes were identified from the diploid woodland strawberry genome.  The phylogenetic tree divides the FvLOX gene into two subfamilies: 9-LOX and 13-LOX.  Gene duplication event analysis showed that whole-genome duplication (WGD)/segmental duplication and dispersed duplication effectively promoted the expansion of strawberry LOX family.  QRT-PCR analysis showed that FvLOX genes were expressed in different tissues.  Expression profile analysis showed that FvLOX1 and FvLOX8 were up-regulated under low temperature stress, FvLOX3 and FvLOX7 were up-regulated under drought stress, FvLOX6 and FvLOX9 were up-regulated under salt stress, FvLOX2, FvLOX3 and FvLOX6 were up-regulated under salicylic acid (SA) treatment, FvLOX3, FvLOX11 and FvLOX14 were up-regulated under methyl jasmonate (MeJA) treatment, FvLOX4 and FvLOX14 were up-regulated under abscisic acid (ABA) treatment.  Promoter analysis showed that FvLOX genes were involved in plant growth and development and stress response.  We analyzed and identified the whole genome of strawberry FvLOX family and characterized a variety of FvLOX candidate genes involved in abiotic stress response.  This study laid a theoretical and empirical foundation for the response mechanism of strawberry to abiotic stress.
Keywords:  lipoxygenase        gene family        strawberry        abiotic stress        expression pattern        cis-acting element  
Received: 07 May 2021   Accepted: 24 August 2021
Fund: This work was supported by the Science and Technology Innovation Fund of Fujian Agriculture and Forestry University (KHF200005).
About author:  LI Zhi-qi, E-mail: zhiqili@fafu.edu.cn; Correspondence CHEN Jian-qing, E-mail: JianqingChen@fafu.edu.cn; CHEN qing-xi, Tel/Fax: +86-591-83789299, E-mail: cqx0246@fafu.edu.cn

Cite this article: 

LI Zhi-qi, Xie Qian, YAN Jia-hui, CHEN Jian-qing, CHEN Qing-xi. 2022. Genome-wide identification and characterization of the abiotic-stress-responsive lipoxygenase gene family in diploid woodland strawberry (Fragaria vesca). Journal of Integrative Agriculture, 21(7): 1982-1996.

Andreou A, Brodhun F, Feussner I. 2009. Biosynthesis of oxylipins in non-mammals. Progress in Lipid Research, 3–4, 148–170.
Andriy P, Jackie W, Brian J, Chris W. 2010. Identification of the lipoxygenase gene family from Vitis vinifera and biochemical characterisation of two 13-lipoxygenases expressed in grape berries of Sauvignon Blanc. Functional Plant Biology, 37, 767–784.
Bailey T L, Johnson J, Grant C E, Noble W S. 2015. The MEME suite. Nucleic Acids Research, 43, W39–W49.
Bailly C, Bogatek-Leszczynska R, Côme D, Corbineau F. 2002. Changes in activities of antioxidant enzymes and lipoxygenase during growth of sunflower seedlings from seeds of different vigour. Seed Science Research, 12, 47–55.
Bannenberg G, Martínez M, Hamberg M, Castresana C. 2009. Diversity of the enzymatic activity in the lipoxygenase gene family of Arabidopsis thaliana. Lipids, 44, 85–95.
Barry C S, Giovannoni J J. 2007. Ethylene and fruit ripening. Journal of Plant Growth Regulation, 26, 143–159.
Bell E, Creelman R A, Mullet J E. 1995. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 92, 8675–8679.
Bell E, Mullet J E. 1993. Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiology, 103, 1133–1137.
Blée E. 2002. Impact of phyto-oxylipins in plant defense. Trends in Plant Science, 7, 315–322.
Brash A R. 1999. Lipoxygenases: Occurrence, functions, catalysis, and acquisition of substrate. Journal of Biological Chemistry, 274, 23679–23682.
Browse J. 2009. Jasmonate passes muster: A receptor and targets for the defense hormone. Annual Review of Plant Biology, 60, 183–205.
Chen C, Chen H, Zhang Y, Thomas H R, Frank M H, He Y, Xia R. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13, 1194–1202.
Chen Z, Chen X, Yan H, Li W, Li Y, Cai R, Xiang Y. 2015. The lipoxygenase gene family in poplar: Identification, classification, and expression in response to MeJA treatment. PLoS ONE, 10, e0125526.
Chuck G. 2010. Molecular mechanisms of sex determination in monoecious and dioecious plants. Advances in Botanical Research, 54, 53–83.
Duan Y B, Li J, Qin R Y, Xu R F, Li H, Yang Y C, Ma H, Li L, Wei P C, Yang J B. 2015. Identification of a regulatory element responsible for salt induction of rice OsRAV2 through ex situ and in situ promoter analysis. Plant Molecular Biology, 90, 49–62.
Dunn M A, White A J, Vural S, Hughes M A. 1998. Identification of promoter elements in a low-temperature-responsive gene (blt4.9) from barley (Hordeum vulgare L.). Plant Molecular Biology, 38, 551–564.
Edger P P, Poorten T J, VanBuren R, Hardigan M A, Colle M, McKain M R, Smith R D, Teresi S J, Nelson A D L, Wai C M, Alger E I, Bird K A, Yocca A E, Pumplin N, Ou S, Ben-Zvi G, Brodt A, Baruch K, Swale T, Shiue L, et al. 2019. Origin and evolution of the octoploid strawberry genome. Nature Genetics, 51, 541–547.
Finn R D, Coggill P, Eberhardt R Y, Eddy S R, Mistry J, Mitchell A L, Potter S C, Punta M, Qureshi M, Sangrador-Vegas A, Salazar G A, Tate J, Bateman A. 2016. The Pfam protein families database: Towards a more sustainable future. Nucleic Acids Research, 44, D279–D285.
Gouinguené S P, Turlings T C. 2002. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiolgy, 29, 1296–1307.
Grebner W, Stingl N E, Oenel A, Mueller M J, Berger S. 2013. Lipoxygenase6-dependent oxylipin synthesis in roots is required for abiotic and biotic stress resistance of Arabidopsis. Plant Physiology, 161, 2159–2170.
Guo A Y, Zhu Q H, Chen X, Luo J C. 2007. GSDS: A gene structure display server. Hereditas, 29, 1023–1026.
Hobo T, Asada M, Kowyama Y, Hattori T. 1999. ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. The Plant Journal, 19, 679–689.
Hoffmann T, Kalinowski G, Schwab W. 2006. RNAi-induced silencing of gene expression in strawberry fruit (Fragaria × ananassa) by agroinfiltration: A rapid assay forgene function analysis. The Plant Journal, 48, 818–826.
Hornung E, Walther M, Kühn H, Feussner I. 1999. Conversion of cucumber linoleate 13-lipoxygenase to a 9-lipoxygenating species by site-directed mutagenesis. Proceedings of the National Academy of Sciences of the United States of America, 96, 4192–4197.
Hou Y, Meng K, Han Y, Ban Q, Wang B, Suo J, Lv J, Rao J. 2015. The persimmon 9-lipoxygenase gene DkLOX3 plays positive roles in both promoting senescence and enhancing tolerance to abiotic stress. Frontiers in Plant Science, 6, 1073.
Hui D, J B, Wu Q, Zhang S Z, Chen L, Dai Y S, Wang D F, Du J J, Xiao S, Yang C W. 2016. Jasmonate complements the function of Arabidopsis lipoxygenase3 in salinity stress response. Plant Science, 244, 1–7.
IPGI (International Peach Genome Initiative), Verde I, Abbott A G, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori M T, Grimwood J, Cattonaro F, Zuccolo A, Rossini L, Jenkins J, Vendramin E, Meisel L A, Decroocq V, Sosinski B, Prochnik S, Mitros T, et al. 2013. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nature Genetics, 45, 487–494.
Jiao Y, Wickett N J, Ayyampalayam S, Chanderbali A S, Landherr L, Ralph P E, Tomsho L P, Hu Y, Liang H, Soltis P S, Soltis D E, Clifton S W, Schlarbaum S E, Schuster S C, Ma H, Leebens-Mack J, dePamphilis C W. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature, 473, 97–100.
Kolomiets M V, Hannapel D J, Chen H, Tymeson M, Gladon R J. 2001. Lipoxygenase is involved in the control of potato tuber development. Plant Cell, 13, 613–626.
Kumar M, Lee S C, Kim J K, Kim S J, Aye S S, Kim S R. 2014. Over-expression of dehydrin gene, OsDhn1, improves drought and salt stress tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). Journal of Plant Biology, 57, 383–393.
Lee T H, Tang H, Wang X, Paterson A H. 2013. PGDD: A database of gene and genome duplication in plants. Nucleic Acids Research, 41, D1152–D1158.
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé 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 Research, 30, 325–327.
Letunic I, Bork P. 2016. Interactive tree of life (iTOL) v3: An online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Research, 44, W242–W245.
Li M, Li L, Dunwell J M, Qiao X, Liu X, Zhang S. 2014. Characterization of the lipoxygenase (LOX) gene family in the Chinese white pear (Pyrus bretschneideri) and comparison with other members of the Rosaceae. BMC Genomics, 15, 444.
Lim C W, Han S W, Hwang I S, Kim D S, Hwang B K, Lee S C. 2015. The pepper lipoxygenase CaLOX1 plays a role in osmotic, drought and high salinity stress response. Plant Cell Physiology, 56, 930–942.
Liu J P, Zhou Y, Li J W, Wang F, Yang Y X. 2020. Comprehensive genomic characterization and expression analysis of the lipoxygenase gene family in watermelon under hormonal treatments. Agriculture, 10, 429. 
Moran P J, Thompson G A. 2001. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiology, 125, 1074–1085.
Nafie E, Hathout T, Al Mokadem S. 2011. Jasmonic acid elicits oxidative defense and detoxification systems in Cucumis melo L. cells. Brazilian Journal of Plant Physiology, 2, 161–174.
Narusaka Y, Nakashima K, Shinwari Z K, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K. 2003. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. The Plant Journal, 34, 137–148.
Raymond O, Gouzy J, Just J, Badouin H, Verdenaud M, Lemainque A, Vergne P, Moja S, Choisne N, Pont C, Carrère S, Caissard J C, Couloux A, Cottret L, Aury J M, Szécsi J, Latrasse D, Madoui M A, François L, Fu X, et al. 2018. The Rosa genome provides new insights into the domestication of modern roses. Nature Genetics, 50, 772–777.
Rodgers-Melnick E, Mane S P, Dharmawardhana P, Slavov G T, Crasta O R, Strauss S H, Brunner A M, Difazio S P. 2012. Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus. Genome Research, 22, 95–105.
Schmittgen T D, Livak K J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101–1108.
Shaban M, Ahmed M M, Sun H, Ullah A, Zhu L. 2018. Genome-wide identification of lipoxygenase gene family in cotton and functional characterization in response to abiotic stresses. BMC Genomics, 19, 599.
Shibata D, Axelrod B. 1995. Plant lipoxygenases. Journal of Lipid Mediators and Cell Signalling, 12, 213–228.
Shulaev V, Sargent D J, Crowhurst R N, Mockler T C, Folkerts O, Delcher A L, Jaiswal P, Mockaitis K, Liston A, Mane S P, Burns P, Davis T M, Slovin J P, Bassil N, Hellens R P, Evans C, Harkins T, Kodira C, Desany B, Crasta O R, et al. 2011. The genome of woodland strawberry (Fragaria vesca). Nature Genetics, 43, 109–116.
Storozhenko S, De Pauw P, Van Montagu M, Inzé D, Kushnir S. 1998. The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant and Cell Physiology, 118, 1005–1014.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
Umate P. 2011. Genome-wide analysis of lipoxygenase gene family in Arabidopsis and rice. Plant Signaling and Behavior, 6, 335–338.
Upadhyay R K, Mattoo A K. 2018. Genome-wide identification of tomato (Solanum lycopersicum L.) lipoxygenases coupled with expression profiles during plant development and in response to methyl-jasmonate and wounding. Journal of Plant Physiology, 231, 318–328.
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar S K, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, et al. 2010. The genome of the domesticated apple (Malus × domestica Borkh.). Nature Genetics, 42, 833–839.
Vellosillo T, Martínez M, López MA, Vicente J, Cascón T, Dolan L, Hamberg M, Castresana C. 2007. Oxylipins produced by the 9-lipoxygenase pathway in Arabidopsis regulate lateral root development and defense responses through a specific signaling cascade. Plant Cell, 19, 831–846.
Wang J, Hu T, Wang W, Hu H, Wei Q, Wei X, Bao C. 2019. Bioinformatics analysis of the lipoxygenase gene family in radish (Raphanus sativus) and functional characterization in response to abiotic and biotic stresses. International Journal of Molecular Sciences, 20, 6095.
Wang Y, Tang H, Debarry J D, Tan X, Li J, Wang X, Lee T H, Jin H, Marler B, Guo H, Kissinger J C, Paterson A H. 2012. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 40, e49.
Wei W, Hu Y, Cui M Y, Han Y T, Gao K, Feng J Y. 2016. Identification and transcript analysis of the TCP transcription factors in the diploid woodland strawberry Fragaria vesca. Frontiers in Plant Science, 7, 1937.
Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan M A, Tao S, Korban S S, Wang H, Chen N J, Nishio T, Xu X, Cong L, Qi K, Huang X, Wang Y, Zhao X, Wu J, Deng C, et al. 2013. The genome of the pear (Pyrus bretschneideri Rehd.). Genome Research, 23, 396–408.
Zhang B, Chen K, Bowen J, Allan A, Espley R, Karunairetnam S, Ferguson I. 2006. Differential expression within the LOX gene family in ripening kiwifruit. Journal of Experimental Botany, 57, 3825–3836.
Zhang Q, Chen W, Sun L, Zhao F, Huang B, Yang W, Tao Y, Wang J, Yuan Z, Fan G, Xing Z, Han C, Pan H, Zhong X, Shi W, Liang X, Du D, Sun F, Xu Z, Hao R, et al. 2012. The genome of Prunus mume. Nature Communications, 3, 1318.

[1] HOU Qian-dong, HONG Yi, WEN Zhuang, SHANG Chun-qiong, LI Zheng-chun, CAI Xiao-wei, QIAO Guang, WEN Xiao-peng. Molecular characterization of the SAUR gene family in sweet cherry and functional analysis of PavSAUR55 in the process of abscission[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1720-1739.
[2] LI Sheng-lan, TAN Ting-ting, FAN Yuan-fang, Muhammad Ali RAZA, WANG Zhong-lin, WANG Bei-bei, ZHANG Jia-wei, TAN Xian-ming, CHEN Ping, Iram SHAFIQ, YANG Wen-yu, YANG Feng. Response of leaf stomatal and mesophyll conductance to abiotic stress factors[J]. >Journal of Integrative Agriculture, 2022, 21(10): 2787-2804.
[3] SHI Bei-bei, WANG Juan, GAO Hai-feng, ZHANG Xiao-juan, WANG Yang, MA Qing. The TaFIM1 gene mediates wheat resistance against Puccinia striiformis f. sp. tritici and responds to abiotic stress[J]. >Journal of Integrative Agriculture, 2021, 20(7): 1849-1857.
[4] WANG Xi-cheng, WU Wei-min, ZHOU Bei-bei, WANG Zhuang-wei, QIAN Ya-ming, WANG Bo, YAN Li-chun. Genome-wide analysis of the SCPL gene family in grape (Vitis vinifera L.)[J]. >Journal of Integrative Agriculture, 2021, 20(10): 2666-2679.
[5] MIAO Li-li, LI Yu-ying, ZHANG Hong-juan, ZHANG Hong-ji, LIU Xiu-lin, WANG Jing-yi, CHANG Xiao-ping, MAO Xin-guo, JING Rui-lian. TaSnRK2.4 is a vital regulator in control of thousand-kernel weight and response to abiotic stress in wheat[J]. >Journal of Integrative Agriculture, 2021, 20(1): 46-54.
[6] HUANG Cong, LANG Kun, QIAN Wan-qiang, WANG Shu-ping, CAO Xiao-mei, HE Rui, ZHAN An-ran, CHEN Meng-yao, YANG Nian-wan, LI Fei. InvasionDB: A genome and gene database of invasive alien species[J]. >Journal of Integrative Agriculture, 2021, 20(1): 191-200.
[7] QIN Jin-xia, JIANG Yu-jie, LU Yun-ze, ZHAO Peng, WU Bing-jin, LI Hong-xia, WANG Yu, XU Sheng-bao, SUN Qi-xin, LIU Zhen-shan. Genome-wide identification and transcriptome profiling reveal great expansion of SWEET gene family and their wide-spread responses to abiotic stress in wheat (Triticum aestivum L.)[J]. >Journal of Integrative Agriculture, 2020, 19(7): 1704-1720.
[8] WANG Yi-fan, LIAO Yu-qiu, WANG Ya-peng, YANG Jiang-wei, ZHANG Ning, SI Huai-jun. Genome-wide identification and expression analysis of StPP2C gene family in response to multiple stresses in potato (Solanum tuberosum L.)[J]. >Journal of Integrative Agriculture, 2020, 19(6): 1609-1624.
[9] FANG Zheng-wu, HE Yi-qin, LIU Yi-ke, JIANG Wen-qiang, SONG Jing-han, WANG Shu-ping, MA Dong-fang, YIN Jun-liang. Bioinformatic identification and analyses of the non-specific lipid transfer proteins in wheat[J]. >Journal of Integrative Agriculture, 2020, 19(5): 1170-1185.
[10] LI Wei-hua, LIU Qi-zhi. Changes in fungal community and diversity in strawberry rhizosphere soil after 12 years in the greenhouse[J]. >Journal of Integrative Agriculture, 2019, 18(3): 677-687.
[11] ZHANG Ya-bin, TANG Wei, WANG Li-huan, HU Ya-wen, LIU Xian-wen, LIU Yong-sheng. Kiwifruit (Actinidia chinensis) R1R2R3-MYB transcription factor AcMYB3R enhances drought and salinity tolerance in Arabidopsis thaliana[J]. >Journal of Integrative Agriculture, 2019, 18(2): 417-427.
[12] GUO Yuan, XU Chang-bing, SUN Xian-jun, HU Zheng, FAN Shou-jin, JIANG Qi-yan, ZHANG Hui. TaSAUR78 enhances multiple plant abiotic stress responses by regulating the interacting gene TaVDAC1[J]. >Journal of Integrative Agriculture, 2019, 18(12): 2682-2690.
[13] ZHAO Bing-ru, FU Xue-feng, TIAN Ke-chuan, HUANG Xi-xia, DI Jiang, BAI Yan, XU Xin-ming, TIAN Yue-zhen, WU Wei-wei, ABLAT Sulayman, ZENG Wei-dan, HANIKEZI Tulafu. Identification of SNPs and expression patterns of FZD3 gene and its effect on wool traits in Chinese Merino sheep (Xinjiang Type)[J]. >Journal of Integrative Agriculture, 2019, 18(10): 2351-2360.
[14] WANG Ling-shuang, CHEN Qing-shan, XIN Da-wei, QI Zhao-ming, ZHANG Chao, LI Si-nan, JIN Yang-mei, LI Mo, MEI Hong-yao, SU An-yu, WU Xiao-xia. Overexpression of GmBIN2, a soybean glycogen synthase kinase 3 gene, enhances tolerance to salt and drought in transgenic Arabidopsis and soybean hairy roots[J]. >Journal of Integrative Agriculture, 2018, 17(09): 1959-1971.
[15] LIU Zheng-jie, ZHAO Yan-peng, ZENG Ling-he, ZHANG Yuan, WANG Yu-mei, HUA Jin-ping. Characterization of GhSERK2 and its expression associated with somatic embryogenesis and hormones level in Upland cotton[J]. >Journal of Integrative Agriculture, 2018, 17(03): 517-529.
No Suggested Reading articles found!