植物雌雄异株性别决定研究进展

doi:10.17520/biods.2021416

生物多样性 ›› 2022, Vol. 30 ›› Issue (3): 21416. DOI: 10.17520/biods.2021416

植物雌雄异株性别决定研究进展

彭丹¹, 武志强¹^,²^,^*()

1.岭南现代农业科学与技术广东省实验室深圳分中心, 农业农村部农业基因数据分析重点实验室, 中国农业科学院(深圳)农业基因组研究所, 广东深圳 518124
2.佛山鲲鹏现代农业研究院, 广东佛山 528200

收稿日期:2021-10-19 接受日期:2021-12-23 出版日期:2022-03-20 发布日期:2022-03-10
通讯作者: 武志强
作者简介:*E-mail: wuzhiqiang@caas.cn
基金资助:
深圳市优秀科技创新人才培养-优秀青年基础研究(RCYX20200714114538196);中国农业科学院深圳农业基因组研究所启动资金(SJXW19073)

Progress on sex determination of dioecious plants

Dan Peng¹, Zhiqiang Wu¹^,²^,^*()

1 Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, Guangdong 518124
2 Kunpeng Institute of Modern Agriculture at Foshan, Foshan, Guangdong 528200

Received:2021-10-19 Accepted:2021-12-23 Online:2022-03-20 Published:2022-03-10
Contact: Zhiqiang Wu

摘要/Abstract

摘要：

植物中雌雄性别分化是一种进化的性状。雌雄异株在多个开花植物谱系中独立演化, 但各个支系的性染色体状态、性别决定区域与性别决定基因不尽相同。多样的植物性染色体和性别决定系统为研究植物性别相关基因的形成机制、性别决定区域和性染色体进化提供了极好的机会。随着测序技术的进步和分析方法的提高, 近年来越来越多物种性别决定的相关分子机制得到解析, 并将理论成果应用于提升经济效益与城市环境等实际问题中。本文将从目前的研究现状和方法, 性别决定单、双基因模型的建立, 植物性染色体进化过程等方面进行总结, 对未来植物性别决定的研究提出四点建议: (1)研究方向逐步从基因研究扩展到调控途径研究; (2)从单一物种转向相关科属比较研究; (3)改进现有性别决定基因模型或探索新模型和性别模式物种; (4)加强性别鉴定技术在实际生产中的研发工作。同时探讨性别决定理论研究未来在农业生产、园艺绿化种植中幼苗性别鉴别筛选等方面的应用前景。

关键词: 雌雄异株, 性别决定, 性染色体, 重组抑制, 双基因模型

Abstract

Background & Aims: Sexual differentiation of plants, also known as dioecy, is the phenomenon of the different female and male reproductive organs in different species and individuals. Dioecious species of flowering plants evolved independently into multiple phylogenetic branches, with each expressing different sex chromosome status, sex determination regions and genes for each branch. In this review, we will summarize the current direction of sex determination research in angiosperms, and appropriately prospect the direction of future research.

Progress: We summarized the formation process of the plant sex determining gene model and the evolution of plant sex chromosomes after conducting a literature review. Two types of mutation models for plant sex determination have been proposed: the ‘two-mutations’ model clarifies that the evolution of sex determination requires two mutations, leading to male sterility and female sterility respectively, while the ‘single-mutation’ model is a single mutant gene that regulates and determines both male and female development of the plant. The diversity of plant sex chromosomes and sex determination systems provides an excellent opportunity to study the formation mechanism of plant sex-related genes, sex determination regions, and sex chromosome evolution. The evolution of plant chromosomes started with a pair of autosomes producing sex-determining gene mutations, forming the initial sex chromosomes. With different selection pressure between female and male plant individuals, the mutant genes were gradually antagonized, and the recombination inhibition was promoted. Accumulation of repeated elements and inhibition of recombination causes the Hill-Robertson effect, which increases the difference between the two chromosomes and eventually leads to the formation of sex chromosomes. The sex chromosomes of some species gradually evolved from homomorphic chromosomes to heteromorphic chromosomes. In this review, sex-determined regions and genes are sorted out and compared in detail according to currently existing characteristics. At present, most studies on the sex-determining regions and genes of angiosperms are carried out by methods such as genome, transcriptome, and resequencing, and the results are primarily in line with the ‘two-mutations’ or ‘single-mutation’ models. Meanwhile, this review further outlines the application of sex determination research in practical production.

Prospects: We propose four suggestions for future research on sex determination in plants: (1) gradually expanding the sight from gene to the regulatory pathways of research; (2) shifting from a single species to research comparisons of related families and genera; (3) improving and exploring current or new sex-determining gene models or sex-model species; and (4) strengthening the identification technology in actual production research and development efforts.

Key words: dioecious plants, sex determination, sex chromosomes, recombination suppression, ‘two-mutations’, model

彭丹, 武志强 (2022) 植物雌雄异株性别决定研究进展. 生物多样性, 30, 21416. DOI: 10.17520/biods.2021416.

Dan Peng, Zhiqiang Wu (2022) Progress on sex determination of dioecious plants. Biodiversity Science, 30, 21416. DOI: 10.17520/biods.2021416.

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链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2021416

https://www.biodiversity-science.net/CN/Y2022/V30/I3/21416

图/表 3

表1 典型代表植物性别决定的研究成果

Table 1 Results of sex determination of representative plants

类群 Taxon	物种 Species	性别决定系统 Sex determination system	性别决定区域或基因 Sex-linked region or genes	同源基因或家族 Ortholog gene or family	参考文献 Reference
苔藓植物 Bryophyte	地钱 Marchantia polymorpha	XY	14个雄性特异性基因 14 male-specific genes	-	Yamato et al, 2007
裸子植物 Gymnosperm	银杏 Ginkgo biloba	ZW	GbMADS18, Gb_15883, Gb_15884, Gb_15885, Gb_15886, Gb_28587	MADS-box (GbMADS18), RR12 (Gb_15883), RR2 (Gb_15884), ELF6 (Gb_15885), AtBAT1 (Gb_15886), AGL8 (Gb_28587)	Zhang et al, 2019; Liao et al, 2020
被子植物 Angiosperm	番木瓜 Carica papaya	XY	MSY4-5Mb, HSY8.1 Mb, XSY3.5 Mb	-	Liu et al, 2004; Wang et al, 2012
	菠菜 Spinacia oleracea	XY	4号连锁群 LG4 (66.98-69.72 cM and 75.48-92.96 cM)	-	Qian et al, 2017; She et al, 2021
	杨梅 Myrica rubra	ZW	59 kb 8号染色体雌性特异性片段 59 kb female-specific region on chromosome 8	-	Jia et al, 2019
	大麻 Cannabis sativa	XY	性染色体 Sex chromosomes	-	Prentout et al, 2020
	蝇子草 Silene latifolia	XY	SlAP3, SlSTM, SlCUC	AP3 (SlAP3), STM (SlSTM), CUC1/CUC2 (SlCUC)	Zluvova et al, 2006; Cegan et al, 2010
	草莓 Fragaria virginiana	ZW	GMEW, RPP0W	GDP-mannose 3,5-epimerase 2 (GMEW), 60S acidic ribosomal protein P0 (RPP0W)	Charlesworth, 2013; Tennessen et al, 2018
	葡萄 Vitis vinifera	XY	VviINP1, VviYABBY3	INP1 (VviINP1), YAB1 (VviYABBY3)	Massonnet et al, 2020
	君迁子 Diospyros lotus	XY	MeGI, OGI	HB40 (MeGI)	Akagi et al, 2020; Xue et al, 2020
	芦笋 Asparagus officinalis	XY	SOFF, aspTDF1	DUF247 (SOFF), TDF1 (aspTDF1)	Harkess et al, 2017, 2020
	猕猴桃 Actinidia chinensis	XY	SyGl, FrBy	ARR24 (SyGl), FAS1 (FrBy)	Akagi et al, 2018, 2019
	杨树 Populus deltoides, P. tremula, P. alba	XY, ZW	FERR-R, FERR, MmS, ARR17	ARR17	Müller et al, 2020; Xue et al, 2020
	柳树 Salix purpurea, S. triandra	ZW	RR	RR9/ARR17	Li et al, 2020; Zhou et al, 2020

表1 典型代表植物性别决定的研究成果

Table 1 Results of sex determination of representative plants

类群 Taxon	物种 Species	性别决定系统 Sex determination system	性别决定区域或基因 Sex-linked region or genes	同源基因或家族 Ortholog gene or family	参考文献 Reference
苔藓植物 Bryophyte	地钱 Marchantia polymorpha	XY	14个雄性特异性基因 14 male-specific genes	-	Yamato et al, 2007
裸子植物 Gymnosperm	银杏 Ginkgo biloba	ZW	GbMADS18, Gb_15883, Gb_15884, Gb_15885, Gb_15886, Gb_28587	MADS-box (GbMADS18), RR12 (Gb_15883), RR2 (Gb_15884), ELF6 (Gb_15885), AtBAT1 (Gb_15886), AGL8 (Gb_28587)	Zhang et al, 2019; Liao et al, 2020
被子植物 Angiosperm	番木瓜 Carica papaya	XY	MSY4-5Mb, HSY8.1 Mb, XSY3.5 Mb	-	Liu et al, 2004; Wang et al, 2012
	菠菜 Spinacia oleracea	XY	4号连锁群 LG4 (66.98-69.72 cM and 75.48-92.96 cM)	-	Qian et al, 2017; She et al, 2021
	杨梅 Myrica rubra	ZW	59 kb 8号染色体雌性特异性片段 59 kb female-specific region on chromosome 8	-	Jia et al, 2019
	大麻 Cannabis sativa	XY	性染色体 Sex chromosomes	-	Prentout et al, 2020
	蝇子草 Silene latifolia	XY	SlAP3, SlSTM, SlCUC	AP3 (SlAP3), STM (SlSTM), CUC1/CUC2 (SlCUC)	Zluvova et al, 2006; Cegan et al, 2010
	草莓 Fragaria virginiana	ZW	GMEW, RPP0W	GDP-mannose 3,5-epimerase 2 (GMEW), 60S acidic ribosomal protein P0 (RPP0W)	Charlesworth, 2013; Tennessen et al, 2018
	葡萄 Vitis vinifera	XY	VviINP1, VviYABBY3	INP1 (VviINP1), YAB1 (VviYABBY3)	Massonnet et al, 2020
	君迁子 Diospyros lotus	XY	MeGI, OGI	HB40 (MeGI)	Akagi et al, 2020; Xue et al, 2020
	芦笋 Asparagus officinalis	XY	SOFF, aspTDF1	DUF247 (SOFF), TDF1 (aspTDF1)	Harkess et al, 2017, 2020
	猕猴桃 Actinidia chinensis	XY	SyGl, FrBy	ARR24 (SyGl), FAS1 (FrBy)	Akagi et al, 2018, 2019
	杨树 Populus deltoides, P. tremula, P. alba	XY, ZW	FERR-R, FERR, MmS, ARR17	ARR17	Müller et al, 2020; Xue et al, 2020
	柳树 Salix purpurea, S. triandra	ZW	RR	RR9/ARR17	Li et al, 2020; Zhou et al, 2020

图1 双基因性别决定模型(改编自Charlesworth (2015))。Step 1: 物种某对常染色体其中一条获得某种性别不育基因突变; Step 2: 另一条染色体获得对应另一种性别不育基因的突变, 形成性染色体前体; Step 3: 不育基因形成连锁, 性染色体初步形成。其中f→SuF为显性突变, M→m为隐性突变, Step 3中Y染色体阴影部分为不育基因形成连锁。

Fig. 1 Sex determination genes of ‘two-mutations’ model (adapted from Charlesworth (2015)). Step 1: One of a pair of autochromosomes has acquired a mutation of a certain sex-sterile gene; Step 2: The other one autochromosome gains the mutation corresponding to another sex sterile gene, forming the precursor of sex chromosome; Step 3: Sterility genes are linked and sex chromosomes are preliminarily formed. ‘f’ to ‘SuF’ is a dominant mutation, and ‘M’ to ‘m’ is a recessive mutation. The shaded part of Y chromosome in Step 3 represents the linkage of sterile genes.

图2 性染色体进化推论(改编自Ming et al (2011))。a, 常染色体; b, 两个性别决定基因形成; c, 性别决定基因连锁, 形成初步性别决定区域; d, 更多性别相关基因连锁, 性别决定区域扩大; e, 由于重复序列累积, Y染色体增长; f, Y染色体退化; PAR, 拟常染色体区域; SDR, 性别决定区域; f→SuF为显性突变, M→m为隐性突变; M2→m2为雄性功能基因的隐性突变。

Fig. 2 Sex chromosome evolution corollary (adapted from Ming et al (2011)). a, Autosomes; b, Two sex-determining genes are formed; c, Sex determination genes are linked, forming a preliminary sex determination region; d, More sex related genes are linked, and the sex-determined region expands; e, The Y chromosome increases due to the accumulation of repeated sequences; f, Y chromosome degeneration; PAR, Pseudoautosomal regions; SDR, Sex-determined area. ‘f’ to ‘SuF’ is a dominant mutation, and ‘M’ to ‘m’ is a recessive mutation. ‘M2’ to ‘m2’ is a recessive mutation of another male functional gene.

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植物雌雄异株性别决定研究进展

Progress on sex determination of dioecious plants

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