ACS11一个新突变类型导致黄瓜只开雄花

doi:10.1016/j.jia.2023.03.003

Journal of Integrative Agriculture ›› 2023, Vol. 22 ›› Issue (11): 3312-3320.DOI: 10.1016/j.jia.2023.03.003

ACS11一个新突变类型导致黄瓜只开雄花

收稿日期:2022-09-30 接受日期:2022-12-29 出版日期:2023-11-20 发布日期:2023-11-08

A novel mutation in ACS11 leads to androecy in cucumber

WANG Jie^{1, 2*}, LI Shuai^{2, 4*}, CHEN Chen^3*, ZHANG Qi-qi^{1, 2}, ZHANG Hui-min¹, CUI Qing-zhi^{3, 6}, CAI Guang-hua^{2, 4}, ZHANG Xiao-peng⁴, CHAI Sen¹, WAN Li², YANG Xue-yong², ZHANG Zhong-hua¹, HUANG San-wen^{4, 5}, CHEN Hui-ming^3#, SUN Jin-jing^2#

¹ College of Horticulture, Qingdao Agricultural University, Qingdao 266109, P.R.China
²State Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
³ Hunan Vegetable Research Institute, Hunan Academy of Agricultural Sciences, Changsha 410125, P.R.China
⁴ Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518124, P.R.China
⁵ Chinese Academy of Tropical Agriculture Sciences, Haikou 571101, P.R.China
⁶College of Horticulture, Hunan Agricultural University, Changsha 410128, P.R.China

Received:2022-09-30 Accepted:2022-12-29 Online:2023-11-20 Published:2023-11-08
About author:#Correspondence SUN Jin-jing, E-mail: sunjinjing@caas.cn; CHEN Hui-ming, E-mail: huiminghm@163.com * These authors contributed equally to this study.
Supported by:
This work was supported by the National Key Research and Development Program of China (2018YFD1000803), National Natural Science Foundation of China (31701933 and 32002036) and the Shandong Provincial Natural Science Foundation (ZR2020QC157).

摘要/Abstract

摘要：

植物的单性花可以有效促进异交，研究单性花的形成和调控机制对于理解植物性别决定过程有重要意义，也为研究者和农业生产者利用杂种优势提供便利。在黄瓜杂交制种过程中，将只开雌花的株系种植于只开雄花的株系周围，可以显著降低制种成本。筛选更多不同基因背景的只开雄花的材料，将增加可用于育种的种质资源。我们基于前期构建的EMS诱变自交系材料“406”的突变体库，发现了一个新的只开雄花的突变体。遗传分析、全基因组重测序和分子标记辅助验证表明，ACS11基因上发生的异义突变第301位丝氨酸（Ser）变为苯丙氨酸（Phe）导致全雄株的产生。体外酶活性测定表明，此突变导致酶活性完全丧失。本研究为黄瓜雄性亲本选育提供了新的种质资源，并为 ACS 酶的催化机理提供了新的认识。

Abstract:

Sex determination in plants gives rise to unisexual flowers. A better understanding of the regulatory mechanism underlying the production of unisexual flowers will help to clarify the process of sex determination in plants and allow researchers and farmers to harness heterosis. Androecious cucumber (Cucumis sativus L.) plants can be used as the male parent when planted alongside a gynoecious line to produce heterozygous seeds, thus reducing the cost of seed production. The isolation and characterization of additional androecious genotypes in varied backgrounds will increase the pool of available germplasm for breeding. Here, we discovered an androecious mutant in a previously generated ethyl methanesulfonate (EMS)-mutagenized library of the cucumber inbred line ‘406’. Genetic analysis, whole-genome resequencing, and molecular marker-assisted verification demonstrated that a nonsynonymous mutation in the ethylene biosynthetic gene 1-AMINOCYCLOPROPANE-1-CARBOXYLATE SYNTHASE 11 (ACS11) conferred androecy. The mutation caused an amino acid change from serine (Ser) to phenylalanine (Phe) at position 301 (S301F). In vitro enzyme activity assays revealed that this S301F mutation leads to a complete loss of enzymatic activity. This study provides a new germplasm for use in cucumber breeding as the androecious male parent, and it offers new insights into the catalytic mechanism of ACS enzymes.

Key words: cucumber , androecy , ethylene , marker-assisted breeding

WANG Jie, LI Shuai, CHEN Chen, ZHANG Qi-qi, ZHANG Hui-min, CUI Qing-zhi, CAI Guang-hua, ZHANG Xiao-peng, CHAI Sen, WAN Li, YANG Xue-yong, ZHANG Zhong-hua, HUANG San-wen, CHEN Hui-ming, SUN Jin-jing. ACS11一个新突变类型导致黄瓜只开雄花[J]. Journal of Integrative Agriculture, 2023, 22(11): 3312-3320.

WANG Jie, LI Shuai, CHEN Chen, ZHANG Qi-qi, ZHANG Hui-min, CUI Qing-zhi, CAI Guang-hua, ZHANG Xiao-peng, CHAI Sen, WAN Li, YANG Xue-yong, ZHANG Zhong-hua, HUANG San-wen, CHEN Hui-ming, SUN Jin-jing. A novel mutation in ACS11 leads to androecy in cucumber[J]. Journal of Integrative Agriculture, 2023, 22(11): 3312-3320.

参考文献

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.

Boualem A, Fergany M, Fernandez R, Troadec C, Martin A, Morin H, Sari M A, Collin F, Flowers J M, Pitrat M, Purugganan M D, Dogimont C, Bendahmane A. 2008. A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons. Science, 321, 836-844.

Boualem A, Troadec C, Camps C, Lemhemdi A, Morin H, Sari M A, Fraenkel-Zagouri R, Kovalski I, Dogimont C, Perl-Treves R, and Bendahmane A. 2015a. A cucurbit androecy gene reveals how unisexual flowers develop and dioecy emerges. Science, 350, 688-691.

Boualem A, Troadec C, Kovalski I, Sari M A, Perl-Treves R, and Bendahmane A. 2009. A conserved ethylene biosynthesis enzyme leads to andromonoecy in two cucumis species. Plos One, 4, e6144.

Bulens I, Poel B v d, Hertog M L A T M, Proft M P d, Geeraerd A H, Nicolai B M. 2011. Protocol: an updated integrated methodology for analysis of metabolites and enzyme activities of ethylene biosynthesis. Plant Methods, 7, 17.

Chen C, Cui Q Z, Huang S W, Wang S H, Liu X H, Lu X Y, Chen H M, Tian Y. 2018. An EMS mutant library for cucumber. Journal of Integrative Agriculture, 17, 1612-1619.

Chen H M, Sun J J, Li S, Cui Q Z, Zhang H M, Xin F J, Wang H S, Lin T, Gao D L, Wang S H, Li X, Wang D H, Zhang Z H, Xu Z H, Huang S W. 2016. An ACC oxidase gene essential for cucumber carpel development. Molecular Plant, 9, 1315-1327.

García A, Aguado E, Garrido D, Martinez C, Jamilena M. 2020. Two androecious mutations reveal the crucial role of ethylene receptors in the initiation of female flower development in Cucurbita pepo. Plant Journal, 103, 1548-1560.

García A, Aguado E, Martínez C, Loska D, Beltrán S, Valenzuela J L, Garrido D, Jamilena M. 2019. The ethylene receptors CpETR1A and CpETR2B cooperate in the control of sex determination in Cucurbita pepo. Journal of Experimental Botany, 71, 154-167.

Hu B W, Li D W, Liu X, Qi J J, Gao D L, Zhao S Q, Huang S W, Sun J J, Yang L. 2017. Engineering Non-transgenic Gynoecious Cucumber Using an Improved Transformation Protocol and Optimized CRISPR/Cas9 System. Molecular Plant, 10, 1575-1578.

Huai Q, Xia Y, Chen Y, Callahan B, Li N, Ke H. 2001. Crystal structures of 1-aminocyclopropane-1-carboxylate (ACC) synthase in complex with aminoethoxyvinylglycine and pyridoxal-5'-phosphate provide new insight into catalytic mechanisms. Journal of Biological Chemistry, 276, 38210-38216.

Kubicki B. 1969a. Investigation of sex determination in cucumber (Cucumis sativus L.). V. Genes controlling intensity of femaleness. Genetica Polonica, 10, 69-86.

Kubicki B. 1969b. Investigations on sex determination in cucumber (Cucumis sativus L.). VI. Androecism. Genetica Polonica, 10, 87-99.

Kubicki B. 1969c. Investigation of sex determination in cucumber (Cucumis sativus L.). VII. Andromonoecism and hermaphroditism. Genetica Polonica, 10, 101-121.

Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.

Li Q, Li H B, Huang W, Xu Y C, Zhou Q, Wang S H, Ruan J, Huang S W, Zhang Z H. 2019. A chromosome-scale genome assembly of cucumber (Cucumis sativus L.). GigaScience, 8, giz072.

Ma W J, Pannell J R. 2016. Sex determination: separate sexes are a double turnoff in melons. Current Biologoy, 26, R171-R174.

Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, Morin H, Pitrat M, Dogimont C, Bendahmane A. 2009. A transposon-induced epigenetic change leads to sex determination in melon. Nature, 461, 1135-1138.

Neff M M. 1998. dCAPS, a simple technique for the genetic analysis of singlenucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant Journal, 14, 387–392.

Saito S, Fujii N, Miyazawa Y, Yamasaki S, Matsuura S, Mizusawa H, Fujita Y, Takahashi H. 2007. Correlation between development of female flower buds and expression of the CS-ACS2 gene in cucumber plants. Journal of Experimental Botany, 58, 2897-2907.

Sun L F, Dong H, Nasrullah Mei Y Y, Wang N N. 2016. Functional investigation of two 1-aminocyclopropane-1-carboxylate (ACC) synthase-like genes in the moss Physcomitrella patens. Plant Cell Reports, 35, 817-830.

Tanurdzic M, Banks J A. 2004. Sex-determining mechanisms in land plants. The Plant Cell, 16, S61-S71.

Xu C, Hao B W, Sun G L, Mei Y Y, Sun L F, Sun Y M, Wang Y B, Zhang Y Y, Zhang W, Zhang M Y, Zhang Y, Wang D, Rao Z H, Li X, Shen Q J, Wang N N. 2021. Dual activities of ACC synthase: Novel clues regarding the molecular evolution of ACS genes. Science Advances, 7, eabg8752.

Zhang H M, Li S, Yang L, Cai G H, Chen H M, Gao D L, Lin T, Cui Q Z, Wang, D H, Li Z, Cai R, Bai S N, Lucas W J, Huang S W, Zhang Z H, Sun J J. 2021. Gain-of-function of the 1-aminocyclopropane-1-carboxylate synthase gene ACS1G induces female flower development in cucumber gynoecy. The Plant Cell, 33, 306-321.

Zhang Z H, Mao L Y, Chen H M, Bu F J, Li G C, Sun J J, Li S, Sun H H, Jiao C, Blakely R, Pan J S, Cai R, Luo R B, Van d P Y, Jacobsen E, Fei Z J, Huang S W. 2015. Genome-wide mapping of structural variations reveals a copy number variant that determines reproductive morphology in cucumber. The Plant Cell, 27, 1595-1604.

ACS11一个新突变类型导致黄瓜只开雄花

A novel mutation in ACS11 leads to androecy in cucumber

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