基于SSR分子标记的5个黄花补血草居群花型变异及其遗传效应

doi:10.13866/j.azr.2025.03.10

摘要/Abstract

摘要： 异型花柱植物居群的花型构成与频率是历代交配事件的结果。“同型花柱”是异型花柱变异和演化中频繁出现的一个的花型，常伴随着异型不亲和系统的瓦解和居群遗传多样性的下降。以分布于塔里木盆地南缘，具有类似于“同型花柱”型花（H型）广泛分布的5个黄花补血草（Limonium aureum）居群为研究对象，来探究H型花的形成及对居群产生的影响。通过野外观测及人工控制授粉实验，对居群花型构成和异型花柱综合征进行调查，同时通过SSR分子标记对居群的遗传多样性和遗传结构进行研究。结果表明：（1） ATS居群仅由H型花构成，其余均为长、短花柱和H型花共存的居群，各居群均具有中等程度的遗传多样性水平、花粉柱头形态的二型性和严格的异型不亲和系统，表现为柱头/花粉形态具有异型性的花型间亲和，反之不亲和。（2）遗传结构、主坐标分析及系统发育分析均显示ATS居群在进化上独立于其余4个居群，5个居群被分为两类，且遗传距离和地理距离呈显著相关性。（3）两类居群中的H型花可能处于异型花柱演化的不同阶段，其严格的自交不亲和性维持了各居群的遗传多样性水平。

关键词: 异型花柱, 黄花补血草, 花型变异, 遗传多样性, 同长花柱

Abstract:

In heterostylous plants, the floral morph composition and frequency of populations are a consequence of mating events over generations. “Homostyly” with anthers and stigmas at the same level within a flower is a floral morph that frequently appears in the evolution of heterostyly and is often accompanied by breakdown of the heteromorphic incompatibility system and the decline of genetic diversity. To explore the formation of the H-morph and its effects on the population, we studied five Limonium aureum populations exhibiting a widely distributed floral morph (H-morph), similar to “homostyly,” in the southern margin of Tarim Basin. The floral morph composition and heterostylous syndrome were investigated by field observations and hand pollination experiments. Meanwhile, the genetic diversity and genetic structure were studied using SSR molecular markers. The results showed the following: (1) The Atushi (ATS) population consisted only of the H-morph, while the remaining four populations were composed of the long- and short-styled morph, and H-morph. All populations had a moderate level of genetic diversity, dimorphism of stigma-pollen morphology, and a strict heteromorphic incompatibility system, revealing that the floral morphs with different pollen ornamentation and stigma papilla cell morphology were compatible. (2) Genetic structure analysis, principal coordinate analysis, and phylogenetic analysis showed that the ATS population had emerged earlier and was independent of the other four populations phylogenetically, with a significant correlation between genetic distance and geographic distance. (3) The H-morphs of the two types of populations may be at different stages of the evolution of heterostyly. The self-incompatibility of the H-morph and the heteromorphic incompatibility system of the population maintained the population’s genetic diversity.

Key words: heterostyly, Limonium aureum, floral variation, genetic diversity, homostyly

张晶, 何爽, 张爱勤. 基于SSR分子标记的5个黄花补血草居群花型变异及其遗传效应[J]. 干旱区研究, 2025, 42(3): 499-510.

ZHANG Jing, HE Shuang, ZHANG Aiqin. Floral morph variation and genetic effect of five Limonium aureum populations based on Simple Sequence Repeat molecular markers[J]. Arid Zone Research, 2025, 42(3): 499-510.

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参考文献 48

[1]	张冬梅, 张华新, 沈熙环, 等. 油松种子园交配系统的时空变化研究[J]. 林业科学, 2004, 40(1): 70-77.
	[Zhang Dongmei, Zhang Huaxin, Shen Xihuan, et al. Study on temporal and spatial change of the mating system in a seed orchard of Pinus tabulaeformis[J]. Scientia Silvae Sinicae, 2004, 40(1): 70-77.]
[2]	Charlesworth D, Wright S I. Breeding systems and genome evolution[J]. Current Opinion in Genetics and Development, 2001, 11(6): 685-690.
[3]	Hamrick J L. Lsozymes and the Analysis of Genetic Structure in Plant Populations[M]. Dordrecht: Springer Netherlands, 1989: 73-86.
[4]	Charlesworth D, Charlesworth B. Inbreeding depression and its evolutionary consequences[J]. Annual Review of Ecology and Systematics, 1987, 18(1): 237-268.
[5]	Fant J B, Havens K, Keller J M, et al. The influence of contemporary and historic landscape features on the genetic structure of the sand dune endemic, Cirsium pitcher (Asteraceae)[J]. Heredity, 2014, 112(5): 519-530. doi: 10.1038/hdy.2013.134 pmid: 24398882
[6]	Young A, Boyle T, Brown T. The population genetic consequences of habitat fragmentation for plants[J]. Trends in Ecology and Evolution, 1996, 11(10): 413-418.
[7]	Leimu R, Mutikainen P, Fischer K M. How general are positive relationships between plant population size, fitness and genetic variation[J]. Journal of Ecology, 2006, 94(5): 942-952.
[8]	Brauner S, Crawford D J, Stuessy T F. Ribosomal DNA and RAPD variation in the rare plant family Lactoridaceae[J]. American Journal of Botany, 1992, 79(12): 1436-1439.
[9]	Darwin C. The Different Forms of Flowers on Plants of the Same Species[M]. London: Murray John, 1877: 244-277.
[10]	Ganders F R. The biology of heterostyly[J]. New Zealand Journal of Botany, 1979, 17(4): 607-635.
[11]	Fisher R A. On the selective consequences of East’s (1927) theory of heterostylism in Lythrum[J]. Journal of Genetics, 1935, 30(3): 369-382.
[12]	Perez-Barrales R, Arroyo J. Pollinator shifts and the loss of style polymorphism in Narcissus papyraceus (Amaryllidaceae)[J]. Journal of Evolutionary Biology, 2010, 23(6): 1117-1128.
[13]	Yuan S, Barrett S C H, Duan T T, et al. Ecological correlates and genetic consequences of evolutionary transitions from distyly to homostyly[J]. Annals of Botany, 2017, 120(5): 775-789. doi: 10.1093/aob/mcx098 pmid: 28961784
[14]	Eckert C G, Barrett S C H. Style morph ratios in tristylous Decodon verticillatus (Lythraceae): Selection vs. historical contingency[J]. Ecology, 1995, 76(4): 1051-1066.
[15]	Husband B C, Barrett S C H. Genetic drift and the maintenance of the style length polymorphism in tristylous populations of Eichhornia paniculate (Pontederiaceae)[J]. Heredity, 1992, 69(5): 440-449.
[16]	Charlesworth D. Primrose homostyles: A classic case of possible balancing selection revisited[J]. Molecular Ecology, 2023, 32(1): 30-32.
[17]	Busch J W, Delph L. The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization[J]. Annals of Botany, 2012, 109(3): 553-562. doi: 10.1093/aob/mcr219 pmid: 21937484
[18]	Matias R, Perez-Barrales R, Consolaro H. Patterns of variation in distylous traits and reproductive consequences in Erythroxylum species and populations[J]. American Journal of Botany, 2020, 107(6): 910-922.
[19]	Barrett S C H. ‘A most complex marriage arrangement’: Recent advances on heterostyly and unresolved questions[J]. New Phytologist, 2019, 224(3): 1051-1067.
[20]	Yuan S, Zeng G, Zhang K, et al. Diverse mating consequences of the evolutionary breakdown of the sexual polymorphism heterostyly[J]. Proceedings of the National Academy of Sciences of the United States of America, 2023, 120(2): e2214492120.
[21]	Hoshino Y, Hoshino M, Yoshioka K, et al. The effects of inbreeding depression and pollinator visitation on the maintenance of herkogamy in Oxalis corniculata, a species derived from a heterostylous ancestor[J]. Plant Species Biology, 2022, 37(6): 349-360.
[22]	Zhong L, Barrett S C H, Wang X J, et al. Phylogenomic analysis reveals multiple evolutionary origins of selfing from outcrossing in a lineage of heterostylous plants[J]. New Phytologist, 2019, 224(3): 1290-1303. doi: 10.1111/nph.15905 pmid: 31077611
[23]	Zhou W, Barrett S C H, Li H D, et al. Phylogeographic insights on the evolutionary breakdown of heterostyly[J]. New Phytologist, 2017, 214(3): 1368-1380. doi: 10.1111/nph.14453 pmid: 28176339
[24]	Zhang W, Hu Y F, He X, et al. Evolution of autonomous selfing in marginal habitats: Spatiotemporal variation in the floral traits of the distylous Primula wannanensis[J]. Frontiers in Plant Science, 2021, 12: 781281.
[25]	Wu L Y, Wang B, Schoen D J, et al. Transitions from distyly to homostyly are associated with floral evolution in the buckwheat genus (Fagopyrum)[J]. American Journal of Botany, 2017, 104(8): 1232-1240.
[26]	Belaoussoff S, Shore J S. Floral correlates and fitness consequences of mating-system variation in Turnera ulmifolia[J]. Evolution, 1995, 49(3): 545-556. doi: 10.1111/j.1558-5646.1995.tb02286.x pmid: 28565088
[27]	Costa J, Torices R, Barrett S C H. Evolutionary history of the buildup and breakdown of the heterostylous syndrome in Plumbaginaceae[J]. New Phytologist, 2019, 224(3): 1278-1289. doi: 10.1111/nph.15768 pmid: 30825331
[28]	Jiménez A, Weigelt B, Santos-Guerra A, et al. Surviving in isolation: Genetic variation, bottlenecks and reproductive strategies in the Canarian endemic Limonium macrophyllum (Plumbaginaceae)[J]. Genetica, 2017, 145(1): 91-104. doi: 10.1007/s10709-017-9948-z pmid: 28108874
[29]	Palop M, Palacios C, González-Candelas F. Development and across-species transferability of microsatellite markers in the genus Limonium (Plumbaginaceae)[J]. Conservation Genetics, 2000, 1(2): 177-179.
[30]	Palop-Esteban M, González-Candelas F. Development of microsatellite markers for the critically endangered Limonium dufourii (Girard) Kuntze (Plumbaginaceae)[J]. Molecular Ecology Resources, 2002, 2(4): 521-523.
[31]	Botstein D, White R L, Skolnick M, et al. Construction of a genetic linkage map in man using restriction fragment length polymorphisms[J]. American Journal of Human Genetics, 1980, 32(3): 314-331. pmid: 6247908
[32]	Koutroumpa K, Theodoridis S, Warren B H, et al. An expanded molecular phylogeny of Plumbaginaceae, with emphasis on Limonium (sea lavenders): Taxonomic implications and biogeographic considerations[J]. Ecology and Evolution, 2018, 8(24): 12397-12424.
[33]	Koutroumpa K, Warren B H, Theodoridis S, et al. Geo-climatic changes and apomixis as major drivers of diversification in the mediterranean sea lavenders (Limonium Mill)[J]. Frontiers in Plant Science, 2021, 11: 612258.
[34]	Baker H G. Dimorphism and monomorphism in the Plumbaginaceae: III. Correlation of geographical distribution patterns with dimorphism and monomorphism in Limonium[J]. Annals of Botany, 1953, 17(4): 615-628.
[35]	Baker H G. Dimorphism and monomorphism in the Plumbaginaceae: I. Survey of the family[J]. Annals of Botany, 1948, 12(3): 207-219.
[36]	Baker H G. The evolution, functioning and breakdown of heteromorphic incompatibility systems. I. The Plumbaginaceae[J]. Evolution, 1966, 20(3): 349-368. doi: 10.1111/j.1558-5646.1966.tb03371.x pmid: 28562969
[37]	杨婉舒, 熊昕, 席党鹏, 等. 乌恰县贝壳山: 塔里木盆地西部沧海桑田的见证者[J]. 自然杂志, 2023, 45(2): 148-154.
	[Yang Wanshu, Xiong Xin, Xi Dangpeng, et al. The transition from sea to land of the western Tarim Basin: Evidence from Shell Mountain of Wuqia County[J]. Chinese Journal of Nature, 2023, 45(2): 148-154.] doi: 10.3969/j.issn.0253-9608.2023.02.010
[38]	潘晓玲. 塔里木盆地植物区系的研究[J]. 新疆大学学报(自然科学版), 1994, 11(4): 77-83.
	[Pan Xiaoling. The study on Tarim Basin Flora[J]. Journal of Xinjiang University (Natural Science), 1994, 11(4): 77-83.]
[39]	欧文雅. 内蒙古境内六种补血草属(Limonium)植物的进化与起源关系初探[D]. 呼和浩特: 内蒙古大学, 2009.
	[Ou Wenya. Preliminary Studies on Evolution and origin of Halophyte Based on Six Species of Limonium in Inner Mongolia[D]. Hohhot: Inner Mongolia University, 2009.]
[40]	Charlesworth B, Charlesworth D. The maintenance and breakdown of distyly[J]. American Naturalist, 1979, 114(4): 499-513.
[41]	Huu C N, Plaschil S, Himmelbach A, et al. Female self-incompatibility type in heterostylous Primula is determined by the brassinosteroid-inactivating cytochrome P450 CYP734A50[J]. Current Biology, 2022, 32(3): 671-676.
[42]	阿依古丽·阿卜杜热伊木, 焦芳芳, 张爱勤. 异型花柱植物喀什补血草的传粉者功能群与花粉转移效率[J]. 植物生态学报, 2021, 45(1): 51-61.
	[Ayiguli·Abudureyimu, Jiao Fangfang, Zhang Aiqin. Pollinator functional groups and their pollen transfer efficiency in heterostylous Limonium kaschgaricum (Plumbaginaceae)[J]. Chinese Journal of Plant Ecology, 2021, 45(1): 51-61.]
[43]	任登芙, 翟雅芯, 张爱勤. 新疆5个驼舌草二型花柱居群交互式雌雄异位的变异[J]. 植物学报, 2023, 58(5): 733-742. doi: 10.11983/CBB22225
	[Ren Dengfu, Zhai Yaxin, Zhang Aiqin. The variation of reciprocal herkogamy in five distylous populations of Goniolimon speciosum in Xinjiang[J]. Chinese Bulletin of Botany, 2023, 58(5): 733-742.]
[44]	Nybom H. Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants[J]. Molecular Ecology, 2004, 13(5): 1143-1155. doi: 10.1111/j.1365-294X.2004.02141.x pmid: 15078452
[45]	Orsini L, Vanoverbeke J, Swillen I, et al. Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization[J]. Molecular Ecology, 2013, 22(24): 5983-5999. doi: 10.1111/mec.12561 pmid: 24128305
[46]	刘硕, Decroocq Veronique, 张玉军, 等. 普通杏和西伯利亚杏野生居群遗传多样性与其地理分布关系研究[J]. 植物遗传资源学报, 2020, 21(6): 1527-1538. doi: 10.13430/j.cnki.jpgr.20200417001
	[Liu Shuo, Decroocq Veronique, Zhang Yujun, et al. Study on the relationship between genetic diversity and geographical distribution of Wild Common Apricots and Siberian Apricots[J]. Journal of Plant Genetic Resources, 2020, 21(6): 1527-1538.]
[47]	Slatkin M. Isolation by distance in equilibrium and non-equilibrium populations[J]. Evolution, 1993, 47(1): 264-279. doi: 10.1111/j.1558-5646.1993.tb01215.x pmid: 28568097
[48]	Zhang J X, Wang M L, Guo Z P, et al. Genetic diversity and population structure of bermudagrass [Cynodon dactylon(L. ) Pers. ] along latitudinal gradients and the relationship with polyploidy level[J]. Diversity, 2019, 11(8): 3-15.

引物名称	上游引物序列（5′→3′）	下游引物序列（5′→3′）	等位基因大小/bp	退火温度/℃
LB6	AGAATCTGAGTGGCTGTT	GGCTTAGGGTTTGTGA	285~290	52
LB12	CAACTGTGAAAGACGGAAAG	CACGGCAATGGAGGAT	212~285	58
LB26	AGAGGGTGCCTGGAAA	AGGGTTGATGGCTTGG	134~140	53
LB30	GTGATAATGCCTGGAGA	GAGGATGTTGGTTTCG	154~180	53
LB64	CAACTGTGAAAGACGGAAAG	CACGGCAATGGAGGAT	212~284	58
Ld081	AACCGACGATCCTCTCTTCTC	AGGATTCGCCGGTCTTGT	144~150	65
Ld445	TCTCTCTCAAGCACCAGCAG	CAGACCGAAGTCAATGAGCA	196~231	60
Ln39	TGAGCCAATTAGGGCCGCTACCGAG	TCAAGACCCAATGGCTCTGCAGCAACAAAA	151	65
Ln149	GAGTGGAAATTAACCGACGGA	CTCCATCCCATCATTATTGTACTCATTGTG	90	55
Ln141	AATTCGATTGCTGCCGAACTG	AATTCATGGACAAGAAGAAGAAGAAGAAGA	189	65
Ln146	CCCGTTCTTCTCTTCCTCCCTTTG	CCATGGATAGATCCCCGCAATTAGCC	196	62
Ln152	CAGCACTTTCTATACTAAAACATCGTCGCC	AATTCGCTGGTGAGCCAACCCTATT	370	65

引物名称	N_a	N_e	I	H_o	H_e	F	F_is	F_st	N_m	PIC
LB12	5.600	2.379	1.168	0.406	0.573	0.307	0.291	0.164	1.272	0.634
LB26	2.200	1.234	0.333	0.125	0.184	0.194	0.318	0.489	0.262	0.270
LB30	2.400	1.674	0.593	0.217	0.363	0.437	0.403	0.445	0.312	0.560
LB6	3.600	1.791	0.719	0.274	0.377	0.308	0.275	0.083	2.771	0.394
LB64	3.600	1.816	0.737	0.330	0.408	0.158	0.190	0.281	0.640	0.470
Ld081	2.800	2.314	0.827	0.533	0.472	-0.106	-0.129	0.375	0.417	0.713
Ld445	2.800	2.322	0.880	0.417	0.536	0.229	0.223	0.318	0.536	0.748
Ln141	3.000	2.392	0.919	0.672	0.554	-0.209	-0.213	0.162	1.296	0.590
Ln146	2.200	1.683	0.610	0.257	0.392	0.411	0.345	0.249	0.755	0.400
Ln152	1.800	1.318	0.257	0.129	0.145	0.251	0.113	0.602	0.166	0.300
Ln39	2.400	1.673	0.379	0.187	0.188	-0.020	0.005	0.344	0.477	0.255
Mean	2.945	1.872	0.675	0.322	0.381	0.178	0.166	0.319	0.809	0.485

居群	N_a	N_e	I	H_o	H_e	F
ATS	2.636	1.833	0.619	0.290	0.360	0.293
MF	2.273	1.581	0.514	0.232	0.304	0.203
NE	3.182	2.154	0.775	0.410	0.439	0.050
WLKSY	3.636	2.105	0.834	0.410	0.455	0.137
YT	3.000	1.688	0.630	0.269	0.346	0.211
Mean	2.945	1.872	0.675	0.322	0.381	0.178

变异来源	自由度	均方和	方差组分	方差分量百分率/%
居群间	4	82.016	0.371	12
居群内	215	557.6929	2.6319	88
总计	219	693.709	3.003	100