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Journal of Integrative Agriculture  2024, Vol. 23 Issue (10): 3506-3521    DOI: 10.1016/j.jia.2024.05.032
Special Issue: 园艺作物基因功能与分子调控机制Horticulture — Gene function · Molecular mechanism
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Enhancer of Shoot Regeneration 2 (ESR2) regulates pollen maturation and vitality in watermelon (Citrullus lanatus)
Hu Wang1, 2, Lihong Cao2, Yalu Guo2, Zheng Li2#, Huanhuan Niu1, 2#

1 College of Horticulture, Henan Agricultural University, Zhengzhou 450002, China

2 State Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling 712100, China

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摘要  西瓜(Citrullus lanatus)作为一种具有高经济价值和营养价值的水果,在全球的水果生产和消费中具有重要意义。探索西瓜雄性生殖发育的调控网络,对开发雄性不育材料和促进西瓜杂交育种具有重要意义。虽然西瓜雄性生殖发育的调控机制对于研究西瓜雄性不育具有重要意义,但目前的相关研究仍较为缺乏。在本研究中,我们确定了APETALA2/乙烯响应因子(AP2/ERF)超家族中VIIIb亚类成员ClESR2是花粉后期发育的关键因子。RNA原位杂交证实,ClESR2在花药发育后期的绒毡层和未成熟的花粉中有显著的表达。进一步的研究发现ClESR2转基因植株的花粉在发育后期表现出形态和活力上的重大缺陷。RNA-seq和蛋白互作分析证实,ClESR2通过在转录和蛋白水平上对绒粘层降解和花粉成熟的相关通路和因子进行调控,影响花粉形态和育性。总之,本研究证实西瓜ClESR2在维持西瓜花粉成熟和活力中起到重要作用。本研究有助于进一步解析西瓜雄性生殖发育过程,为开发西瓜雄性不育材料提供理论依据。

Abstract  
Watermelon (Citrullus lanatus) holds global significance as a fruit with high economic and nutritional value.  Exploring the regulatory network of watermelon male reproductive development is crucial for developing male sterile materials and facilitating cross-breeding.  Despite its importance, there is a lack of research on the regulation mechanism of male reproductive development in watermelon.  In this study, we identified that ClESR2, a VIIIb subclass member in the APETALA2/Ethylene Responsive Factor (AP2/ERF) superfamily, was a key factor in pollen development.  RNA in situ hybridization confirmed significant ClESR2 expression in the tapetum and pollen during the later stage of anther development.  The pollens of transgenic plants showed major defects in morphology and vitality at the late development stage.  The RNA-seq and protein interaction assay confirmed that ClESR2 regulates pollen morphology and fertility by interacting with key genes involved in pollen development at both transcriptional and protein levels.  These suggest that Enhancer of Shoot Regeneration 2 (ESR2) plays an important role in pollen maturation and vitality.  This study helps understand the male reproductive development of watermelon, providing a theoretical foundation for developing male sterile materials.


Keywords:  ESR2        watermelon        overexpression        pollen maturation        pollen vitality  
Received: 23 August 2023   Accepted: 19 April 2024
Fund: 
Thanks for the funding support from the National Key Research and Development Program of China (2022YFD1602000), the National Natural Science Foundation of China (32202514, U22A20498 and 32072596), the Joint Fund of Henan Province Science and Technology Research and Development Plan, China (222103810009), the Science and Technology Innovation Team of Shaanxi, China (2021TD-32), and the China Postdoctoral Science Foundation (2022M711064 and 2023M741062).
About author:  #Correspondence Zheng Li, E-mail: lizheng82@nwsuaf.edu.cn; Huanhuan Niu, E-mail: niuhh@henau.edu.cn

Cite this article: 

Hu Wang, Lihong Cao, Yalu Guo, Zheng Li, Huanhuan Niu. 2024. Enhancer of Shoot Regeneration 2 (ESR2) regulates pollen maturation and vitality in watermelon (Citrullus lanatus). Journal of Integrative Agriculture, 23(10): 3506-3521.

Alexander M P. 1980. A versatile stain for pollen, fungi, yeast and bacteria. Stain Technology, 55, 13–18.

Ariizumi T, Toriyama K. 2011. Genetic regulation of sporopollenin synthesis and pollen exine development. Annual Review of Plant Biology, 62, 437–460.

Bai S L, Peng Y B, Cui J X, Gu H T, Xu L Y, Li Y Q, Xu Z H, Bai S N. 2004. Developmental analyses reveal early arrests of the spore-bearing parts of reproductive organs in unisexual flowers of cucumber (Cucumis sativus L.). Planta, 220, 230–240.

Burnstock G, Verkhratsky A. 2009. Evolutionary origins of the purinergic signalling system. Acta Physiologica, 195, 415–447.

Capua Y, Eshed Y. 2017. Coordination of auxin-triggered leaf initiation by tomato LEAFLESS. Proceedings of the National Academy of Sciences of the United States of America, 114, 3246–3251.

Chandler J W. 2018. Class VIIIb APETALA2 ethylene response factors in plant development. Trends in Plant Science, 23, 151–162.

Chandler J W, Werr W. 2017. DORNRÖSCHEN, DORNRÖSCHEN-LIKE, and PUCHI redundantly control floral meristem identity and organ initiation in Arabidopsis. Journal of Experimental Botany, 68, 3457–3472.

Chen W, Yu X H, Zhang K, Shi J, De Oliveira S, Schreiber L, Shanklin J, Zhang D. 2011. Male Sterile 2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in Arabidopsis. Plant Physiology, 157, 842–853.

Chiu T Y, Christiansen K, Moreno I, Lao J, Loqué D, Orellana A, Heazlewood J L, Clark G, Roux S J. 2012. AtAPY1 and AtAPY2 function as Golgi-localized nucleoside diphosphatases in Arabidopsis thaliana. Plant Cell Physiology, 53, 1913–1925.

Choi H, Jin J Y, Choi S, Hwang J U, Kim Y Y, Suh M C, Lee Y. 2011. An ABCG/WBCtype ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. Plant Journal, 65, 181–193.

Choi H, Ohyama K, Kim Y Y, Jin J Y, Lee S B, Yamaoka Y, Muranaka T, Suh M, Fujioka S, Lee Y. 2014. The role of Arabidopsis ABCG9 and ABCG31 ATP binding cassette transporters in pollen fitness and the deposition of steryl glycosides on the pollen coat. The Plant Cell, 26, 310–324.

Clark G, Brown K A, Tripathy M K, Roux S J. 2021. Recent advances clarifying the structure and function of plant apyrases (nucleoside triphosphate diphosphohydrolases). International Journal of Molecular Sciences, 22, 3283.

Clark G, Morgan R O, Fernandez M P, Salmi M L, Roux S J. 2014. Breakthroughs spotlighting roles for extracellular nucleotides and apyrases in stress responses and growth and development. Plant Science, 225, 107–116.

Day R B, McAlvin C B, Loh J T, Denny R L, Wood T C, Young N D, Stacey G. 2000. Differential expression of two soybean apyrases, one of which is an early nodulin. Molecular Plant (Microbe Interactions), 13, 1053–1070.

Deng S, Sun J, Zhao R, Ding M, Zhang Y, Sun Y, Wang W, Tan Y, Liu D, Ma X, Hou P, Wang M, Lu C, Shen X, Chen S. 2015. Populus euphratica APYRASE2 enhances cold tolerance by modulating vesicular trafficking and extracellular ATP in Arabidopsis plants. Plant Physiology, 169, 530–548.

Dobritsa A A, Shrestha J, Morant M, Pinot F, Matsuno M, Swanson R, Moller B L. Preuss D. 2009. CYP704B1 is a long-chain fatty acid omega-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiology, 151, 574–589.

Herrero A B, Uccelletti D, Hirschberg C B, Dominguez A, Abeijon C. 2002. The Golgi GDPase of the fungal pathogen Candida albicans affects morphogenesis, glycosylation, and cell wall properties. Eukaryotic Cell, 1, 420–431.

Huang M D, Chen T L, Huang A H. 2013. Abundant type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become a constituent of the pollen exine. Plant Physiology, 163, 1218–1229.

Jegadeesan S, Beery A, Altahan L, Meir S, Pressman E, Firon N. 2018. Ethylene production and signaling in tomato (Solanum lycopersicum) pollen grains is responsive to heat stress conditions. Plant Reproduction, 31, 367–383.

Jeong H J, Kang J H, Zhao M, Kwon J K, Choi H S, Bae J H, Lee H A, Joung Y H, Choi D, Kang B C. 2014. Tomato male sterile 1035 is essential for pollen development and meiosis in anthers. Journal of Experimental Botany, 65, 6693–6709.

Jin Y, Pan W, Zheng X, Cheng X, Liu M, Ma H, Ge X. 2018. OsERF101, an ERF family transcription factor, regulates drought stress response in reproductive tissues. Plant Molecular Biology, 98, 51–65.

Knowles A F. 2011. The GDA1_CD39 superfamily: NTPDases with diverse functions. Purinergic Signalling, 7, 21–45.

Li H, Zhang D. 2010. Biosynthesis of anther cuticle and pollen exine in rice. Plant Signaling & Behavior, 5, 1121–1123.

Lim M H, Wu J, Yao J, Gallardo I F, Dugger J W, Webb L J, Huang J, Salmi M L, Song J, Clark G, Roux S J. 2014. Apyrase suppression raises extracellular ATP levels and induces gene expression and cell wall changes characteristic of stress responses. Plant Physiology, 164, 2054–2067.

Liu L, Zhao L, Chen P, Cai H, Hou Z, Jin X, Aslam M, Chai M, Lai L, He Q, Liu Y, Huang X, Chen H, Chen Y, Qin Y. 2020. ATP binding cassette transporters ABCG1 and ABCG16 affect reproductive development via auxin signalling in Arabidopsis. Plant Journal, 102, 1172–1186.

Lou Y, Zhou H S, Han Y, Zeng Q Y, Zhu J, Yang Z N. 2018. Positive regulation of AMS by TDF1 and the formation of a TDF1-AMS complex are required for anther development in Arabidopsis thaliana. New Phytologist, 217, 378–391.

Lu J Y, Xiong S X, Yin W, Teng X D, Lou Y, Zhu J, Zhang C, Gu J N, Wilson Z A, Yang Z N. 2020. MS1, a direct target of MS188, regulates the expression of key sporophytic pollen coat protein genes in Arabidopsis. Journal of Experimental Botany, 71, 4877–4889.

Ma H. 2005. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annual Review of Plant Biology, 56, 393–434.

Morant M, Jorgensen K, Schaller H, Pinot F, Moller B L, Werck-Reichhart D, Bak S. 2007. CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. The Plant Cell, 19, 1473–1487.

Niu H H, Wang H, Zhao B S, He J, Yang L M, Ma X F, Cao J J, Li Z, Shen J J. 2022. Exogenous auxin-induced ENHANCER OF SHOOT REGENERATION 2 (ESR2) enhances femaleness of cucumber by activating CsACS2 gene. Horticulture Research, 9, uhab085.

Nomura Y, Matsuo N, Banno H. 2009. A domain containing the ESR motif in ENHANCER OF SHOOT REGENERATION 1 functions as a transactivation domain. Plant Biotechnology, 26, 395–401.

Rhee S J, Seo M, Jang Y J, Cho S, Lee G P. 2015. Transcriptome profiling of differentially expressed genes in floral buds and flowers of male sterile and fertile lines in watermelon. BMC Genomics, 16, 914.

Riewe D, Grosman L, Fernie A R, Wucke C, Geigenberger P. 2008. The potato-specific apyrase is apoplastically localized and has influence on gene expression, growth, and development. Plant Physiology, 147, 1092–1109.

Shi J, Cui M, Yang L, Kim Y J, Zhang D. 2015. Genetic and biochemical mechanisms of pollen wall development. Trends in Plant Science, 20, 741–753.

Shoji T, Yuan L. 2021. ERF gene clusters: Working together to regulate metabolism. Trends in Plant Science, 26, 23–32.

Steinebrunner I, Wu J, Sun Y, Corbett A, Roux S J. 2003. Disruption of apyrases inhibits pollen germination in Arabidopsis. Plant Physiology, 131, 1638–1647.

Wan X, Wu S, Li Z, An X, Tian Y. 2020. Lipid metabolism: Critical roles in male fertility and other aspects of reproductive development in plants. Molecular Plant, 13, 955–983.

Wang H, Niu H H, Li C, Shen G Y, Liu X F, Weng Y Q, Wu T, Li Z. 2020. WUSCHEL-related homeobox1 (WOX1) regulates vein patterning and leaf size in Cucumis sativus. Horticulture Research, 7, 182.

Wang H, Niu H H, Liang M H, Zhai Y F, Huang W, Ding Q, Du Y, Lu M H. 2019. A wall-associated kinase gene CaWAKL20 from pepper negatively modulates plant thermotolerance by reducing the expression of ABA-responsive genes. Frontiers in Plant Science, 10, 591.

Wang H, Niu H H, Zhai Y F, Lu M H. 2017. Characterization of BiP genes from pepper (Capsicum annuum L.) and the role of CaBiP1 in response to endoplasmic reticulum and multiple abiotic stresses. Frontiers in Plant Science, 8, 1122.

Wang K, Guo Z L, Zhou W T, Zhang C, Zhang Z Y, Lou Y, Xiong S X, Yao X Z, Fan J J, Zhu J, Yang Z N. 2018. The regulation of sporopollenin biosynthesis genes for rapid pollen wall formation. Plant Physiology, 178, 283–294.

Wu J, Steinebrunner I, Sun Y, Butterfield T, Torres J, Arnold D, Gonzalez A, Jacob F, Reichler S, Roux S J. 2007. Apyrases (nucleoside triphosphate-diphosphohydrolases) play a key role in growth control in Arabidopsis. Plant Physiology, 144, 961–975.

Xiong S X, Lu J Y, Lou Y, Teng X D, Gu J N, Zhang C, Shi Q S, Yang Z N, Zhu J. 2016. The transcription factors MS188 and AMS form a complex to activate the expression of CYP703A2 for sporopollenin biosynthesis in Arabidopsis thaliana. Plant Journal, 88, 936–946.

Yang J, Wu J, Romanovicz D, Clark G, Roux S J. 2013. Co-regulation of exine wall patterning, pollen fertility and anther dehiscence by Arabidopsis apyrases 6 and 7. Plant Physiology and Biochemistry, 69, 62–73.

Zhang D, Liang W, Yin C, Zong J, Gu F, Zhang D. 2010. OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiology, 154, 149–162.

Zhang D, Luo X, Zhu L. 2011. Cytological analysis and genetic control of rice anther development. Journal of Genetics and Genomics, 38, 379–390.

Zhang R, Chang J, Li J, Lan G, Xuan C, Li H, Ma J, Zhang Y, Yang J, Tian S, Yuan L, Zhang X, Wei C. 2021. Disruption of the bHLH transcription factor Abnormal Tapetum 1 causes male sterility in watermelon. Horticulture Research, 8, 258.

Zhang X, Zhou Y, Ding L, Wu Z, Liu R, Meyerowitz E M. 2013. Transcription repressor HANABA TARANU controls flower development by integrating the actions of multiple hormones, floral organ specification genes, and GATA3 family genes in Arabidopsis. The Plant Cell, 25, 83–101.

Zheng X, He L, Liu Y, Mao Y, Wang C, Zhao B, Li Y, He H, Guo S, Zhang L, Schneider H, Tadege M, Chan, F, Chen J. 2020. A study of male fertility control in Medicago truncatula uncovers an evolutionarily conserved recruitment of two tapetal bHLH subfamilies in plant sexual reproduction. New Phytologist, 228, 1115–1133.

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