A review of delayed autonomous selfing in flowering plants

doi:10.12302/j.issn.1000-2006.2022008031

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2022, Vol. 46 ›› Issue (6): 233-239.doi: 10.12302/j.issn.1000-2006.2022008031

Special Issue: 南京林业大学120周年校庆特刊

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A review of delayed autonomous selfing in flowering plants

XIAO Hanwen¹(), LIU Qingshan²^,³, TIAN Runan¹^,^*()

1. College of Landscape Architecture, Nanjing Forestry University, Nanjing 210037, China
2. Shanghai Chenshan Botanical Garden, Shanghai 201602, China
3. College of Life Science and Medicine, Zhejiang Sci-Tech University, Hangzhou 310018, China

Received:2022-08-15 Revised:2022-09-25 Online:2022-11-30 Published:2022-11-24
Contact: TIAN Runan E-mail:hwxiao777@163.com;tianrunan@njfu.edu.cn

Abstract

Abstract:

Delayed autonomous self-pollination or delayed selfing is a reproductive way of autonomous self-pollination that occurs at the end of cross-pollination of a single flower in flowering plants. To complement the comprehensive data base of plant evolution and pollination biology, we provide a review of progress in the occurrence pathways, experimental research methods, and the “best of both worlds” reproductive assurance hypothesis of delayed selfing. We also discuss the adaptive significance of delayed selfing and suggest future research directions. The delayed selfing is present in 74 angiosperm species, and widely distributed in 61 genera and 43 families, of which 52 species occur by a single pathway and 22 species by two pathways. In a single pathway, the style curvature is the most common to cause the delayed selfing. Incomplete dichogamy and reduced herkogamy are the most common pathways promoting the delayed selfing occurrence. Observations of delayed selfing have mostly been done through pollination biology, and few studies have combined pollination biology with genetics to provide the most rigorous evidence for the occurrence of delayed selfing. The reproductive assurance hypothesis of delayed selfing suggests that it prioritizes securing cross-pollination and can aid in the reproductive success of plants when the pollination environment is unpredictable. Therefore, the delayed selfing is considered the “best of both worlds” mating system that combines the advantages of selfing and outcrossing. In addition, for ovule-less species, plants have sufficient prior pollination and fertilization after a single visit by insects, which also prevents the occurrence of delayed selfing to save plant resources for other purposes.

Key words: flowering plant, delayed autonomous selfing, reproductive assurance, inbreeding depression, adaptation mechanism

CLC Number:

S718
Q941

XIAO Hanwen, LIU Qingshan, TIAN Runan. A review of delayed autonomous selfing in flowering plants[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2022, 46(6): 233-239.

Figures/Tables 1

Table 1

Species and pathways in which delayed autonomous selfing occurred"

科 family	物种 species	发生途径 pathway	文献 reference
大戟科 Euphorbiaceae	藤状黄蓉花 Dalechampia scandens	雌雄异位程度降低reduced herkogamy	Hildesheheim等^[10]
龙胆科 Gentianaceae	扁蕾 Gentianopsis barbata	雄蕊伸长stamen elongation	段元文等^[19]
龙胆科 Gentianaceae	Prepusa hookeriana	柱头弯曲stigma curvature	Lemos等^[16]
唇形科 Lamiaceae	荫生鼠尾草 Salvia umbratica	柱头弯曲stigma curvature	Xiao等^[12]
	S. hypoleuca		Naghiloo等^[20]
	南欧丹参S. sclarea		Naghiloo等^[20]
狸藻科 Lentibulariaceae	早果狸藻 Utricularia praeterita	雌雄异位程度降低reduced herkogamy	Chaudhary等^[18]
狸藻科 Lentibulariaceae	Utricularia babui	雌雄异位程度降低reduced herkogamy	Chaudhary等^[18]
野牡丹科 Melastomataceae	Bertolonia paranaensis	雌雄异位程度降低和雄蕊运动 reduced herkogamy and stamen movement	Passos等^[21]
野牡丹科 Melastomataceae	B. mosenii	雌雄异位程度降低和雄蕊运动 reduced herkogamy and stamen movement	Passos等^[21]
茄科Solanaceae	天仙子 Hyoscyamus niger	雄蕊伸长stamen elongation	帕丽旦·萨力等^[22]
其中39科	其余63种	单一发生途径:柱头弯曲stigma curvature,雌雄异位程度降低reduced herkogamy,花冠闭合corolla closure,不完全雌雄异熟incomplete dichogamy,花冠脱落corolla abscission,花冠萎蔫corolla wilting,雄蕊伸长stamen elongation,短暂自交不亲和transient self-incompatibility和双柱头diplostigmaty等多途径:不完全雌雄异熟和雌雄异位减小incomplete dichogamy and reduced herkogamy,柱头弯曲和不完全雌雄异熟style curvature and incomplete dichogamy,雌雄异位减小和雄蕊运动reduced herkogamy and stamen movement,短暂自交不亲和和雌雄异位减小transient SI and reduced herkogamy,花冠脱落和柱头弯曲corolla abscission and stigma curavature,不完全雌雄异熟和花丝弯曲incomplete dichogamy and filament curvatur,短暂自交不亲和柱头弯曲transient SI and stigma curvature,花冠脱落和柱头直伸corolla closure and style straightening	Goodwillie等^[8]

Table 1

References 57

[1]	BARRETT S C H. The evolution of plant sexual diversity[J]. Nat Rev Genet, 2002, 3(4):274-284.DOI:10.1038/nrg776.
[2]	OLLERTON J, WINFREE R, TARRANT S. How many flowering plants are pollinated by animals?[J]. Oikos, 2011, 120(3):321-326.DOI:10.1111/j.1600-0706.2010.18644.x.
[3]	LLOYD D G, SCHOEN D J. Self-and cross-fertilization in plants.I.functional dimensions[J]. Int J Plant Sci, 1992, 153(3):358-369.DOI:10.1086/297040.
[4]	LLOYD D G. Some reproductive factors affecting the selection of self-fertilization in plants[J]. Am Nat, 1979, 113(1):67-79.DOI:10.1086/283365.
[5]	LLOYD D G. Self-and cross-fertilization in plants.Ⅱ.the selection of self-fertilization[J]. Int J Plant Sci, 1992, 153(3):370-380.DOI:1058-5893/92/ 5303-0011$02.00.
[6]	HERLIHY C R, ECKERT C G. Genetic cost of reproductive assurance in a self-fertilizing plant[J]. Nature, 2002, 416(6878):320-323.DOI:10.1038/416320a.
[7]	阮成江, 钦佩, 尹增芳. 繁殖保障和延迟自交的研究进展[J]. 生态学报, 2006, 26(1):195-204.
	RUAN C J, QIN P, YIN Z F. Advancements in reproductive assurance and delayed selfing[J]. Acta Ecol Sin, 2006, 26(1):195-204.DOI:10.3321/j.issn:1000-0933.2006.01.026.
[8]	GOODWILLIE C, WEBER J J. The best of both worlds? A review of delayed selfing in flowering plants[J]. Am J Bot, 2018, 105(4):641-655.DOI:10.1002/ajb2.1045.
[9]	ASHMAN T L, SCHOEN D J. How long should flowers live?[J]. Nature, 1994, 371(6500):788-791.DOI:10.1038/371788a0.
[10]	HILDESHEIM L S, et al.OPEDAL Ø H,ARMBRUSTER W S, Fitness costs of delayed pollination in a mixed-mating plant[J]. Ann Bot, 2019, 124(5):869-881.DOI:10.1093/aob/mcz141.
[11]	DELGADO-DÁVILA R, MARTÉN-RODRÍGUEZ S. A test of the reproductive assurance hypothesis in Ipomoea hederacea: does inbreeding depression counteract the benefits of self-pollination?[J]. Am J Bot, 2021, 108(11):2162-2173.DOI:10.1002/ajb2.1794.
[12]	XIAO H W, HUANG Y B, CHANG Y H, et al. Occurrence and prevention of delayed autonomous selfing in Salvia umbratica (Lamiaceae)[J]. Front Plant Sci, 2021, 12:635310.DOI:10.3389/fpls.2021.635310.
[13]	SPIGLER R B, ROSSANA M. Changes in female function and autonomous selfing across floral lifespan interact to drive variation in the cost of selfing[J]. Am J Bot, 2022, 109(4):616-627.DOI:10.1002/ajb2.1816.
[14]	ARATHI H S, RASCH A, COX C, et al. Autogamy and floral longevity in Mimulus guttatus[J]. Int J Plant Sci, 2002, 163(4):567-573.DOI:10.1086/340444.
[15]	CARRIÓ E, HERREROS R, BACCHETTA G, et al. Evidence of delayed selfing in Fumana juniperina (Cistaceae)[J]. Int J Plant Sci, 2008, 169(6):761-767.DOI:10.1086/588070.
[16]	LEMOS A L, MOREIRA M M, BENEVIDES C R, et al. Reproductive biology of Prepusa hookeriana (Gentianaceae):an endangered species of high-altitude grasslands in Brazil[J]. Braz J Bot, 2020, 43(2):379-387.DOI:10.1007/s40415-020-00611-w.
[17]	ZHONG J S, PRESTON J C. Bridging the gaps:evolution and development of perianth fusion[J]. New Phytol, 2015, 208(2):330-335.DOI:10.1111/nph.13517.
[18]	CHAUDHARY A, YADAV S R, TANDON R. Delayed selfing ensures reproductive assurance in Utricularia praeterita and Utricularia babui in Western Ghats[J]. J Plant Res, 2018, 131(4):599-610.DOI:10.1007/s10265-018-1016-y.
[19]	段元文, 何亚平, 张挺锋, 等. 高山植物扁蕾的延迟自交机制[J]. 植物生态学报, 2007, 31(1):110-117.
	DUAN Y W, HE Y P, ZHANG T F, et al. Delayed selfing in an alpine species Gentianopsis barbata[J]. J Plant Ecol, 2007, 31(1):110-117.DOI:10.17521/cjpe.2007.0014.
[20]	NAGHILOO S, NIKZAT-SIAHKOLAEE S, ESMAILLOU Z, et al. Pollination efficiency and pollen limitation in bistaminate vs tetrastaminate Lamiaceae[J]. Plant Species Biol, 2021, 37(1):91-102.DOI: 10.1111/1442-1984.12357.
[21]	PASSOS L, TELLES F, GOLDENBERG R, et al. “Pollen tube shower” in Bertolonia (Melastomataceae):a new delayed selfing mechanism in flowers with poricidal anthers[J]. Bot J Linn Soc, 2021, 198(3):326-341.DOI:10.1093/botlinnean/boab051.
[22]	帕丽旦·萨力, 李新蓉. 天仙子的花部特征及延迟自交机制[J]. 西北植物学报, 2012, 32(10):2009-2015.
	PALIDAN SALI, LI X R. Floral syndrome and delayed autonomous selfing of Hyoscyamus niger[J]. Acta Bot Boreali Occidentalia Sin, 2012, 32(10):2009-2015.DOI:10.3969/j.issn.1000-4025.2012.10.012.
[23]	SEED L, VAUGHTON G, RAMSEY M. Delayed autonomous selfing and inbreeding depression in the Australian annual Hibiscus trionum var.vesicarius (Malvaceae)[J]. Aust J Bot, 2006, 54(1):27-34.DOI:10.1071/BT05017.
[24]	LI Q, RUAN C J, TEIXEIRA DA SILVA J, et al. Floral morphology and mating system of Alcea rosea (Malvaceae)[J]. Plant Ecol Evol, 2012, 145(2):176-184.DOI:10.5091/plecevo.2012.651.
[25]	KLIPS R A, SNOW A A. Delayed autonomous self-pollination in Hibiscus laevis (Malvaceae)[J]. Am J Bot, 1997, 84(1):48-53.DOI:10.2307/2445882.
[26]	BUTTROSE, GRANT W, LOTT J. Reversible curvature of style branches of Hibiscus trionum L.,a pollination mechanism[J]. Aust J Bot, 1977, 25(5):567-570.DOI:10.1071/BT9770567.
[27]	RAMSEY M, SEED L, VAUGHTON G. Delayed selfing and low levels of inbreeding depression in Hibiscus trionum (Malvaceae)[J]. Aust J Bot, 2003, 51(3):275-281.DOI:10.1071/bt02128.
[28]	RUAN C J, ZHOU L J, ZENG F Y, et al. Contribution of delayed autonomous selfing to reproductive success in Kosteletzkya virginica[J]. Belg J Bot, 2008, 141(1):3-13.DOI:10.2307/20794647.
[29]	YE Z M, JIN X F, YANG J, et al. Accurate position exchange of stamen and stigma by movement in opposite direction resolves the herkogamy dilemma in a protandrous plant,Ajuga decumbens (Labiatae)[J]. AoB Plants, 2019, 11(5):plz052.DOI:10.1093/aobpla/plz052.
[30]	阮成江, 姜国斌. 雌雄异位和花部行为适应意义的研究进展[J]. 植物生态学报, 2006, 30(2):210-220.
	RUAN C J, JIANG G B. Adaptive significance of herkogamy and floral behaviour[J]. J Plant Ecol, 2006, 30(2):210-220.DOI:10.17521/cjpe.2006.0030.
[31]	PÉREZ F, ARROYO M T K, ARMESTO J J. Evolution of autonomous selfing accompanies increased specialization in the pollination system of Schizanthus (Solanaceae)[J]. Am J Bot, 2009, 96(6):1168-1176.DOI:10.3732/ajb.0800306.
[32]	LATTOO S K, DHAR R S, KHAN S, et al. Temporal sexual maturation and incremental staminal movement encourages mixed mating in Withania somnifera: an insurance for reproductive success[J]. Current Science, 2007, 92: 1390-1399.
[33]	WANG Y, ZHANG D, RENNER S S, et al. Self-pollination by sliding pollen in Caulokaempferia coenobialis (Zingiberaceae)[J]. Int J Plant Sci, 2005, 166: 753-759. DOI:10.1086/431803.
[34]	KISSLING J, BARRETT S C H. Diplostigmaty in plants:a novel mechanism that provides reproductive assurance[J]. Biol Lett, 2013, 9(5):20130495.DOI:10.1098/rsbl.2013.0495.
[35]	MIRANDA A S, VIEIRA M F. Ruellia subsessilis (Nees) Lindau (Acanthaceae):a species with a sexual reproductive system that responds to different water availability levels[J]. Flora Morphol Distribution Funct Ecol Plants, 2014, 209(12):711-717.DOI:10.1016/j.flora.2014.09.007.
[36]	MAMUT J, LI B, TAN D Y. Protogyny and delayed autonomous self-pollination in the desert herb Zygophyllum macropterum (Zygophyllaceae)[J]. J Syst Evol, 2014, 52(1):75-83.DOI:10.1111/jse.12029.
[37]	DUAN Y W, DAFNI A, HOU Q Z, et al. Delayed selfing in an alpine biennial Gentianopsis paludosa (Gentianaceae) in the Qinghai-Tibetan Plateau[J]. J Integr Plant Biol, 2010, 52 (6):593-599. DOI:10.1111/j.1744-7909.2010.00951.x.
[38]	PAUDEL B R, SHRESTHA M, BURD M, et al. Dual mechanisms of autonomous selfing in Roscoea nepalensis (Zingiberaceae)[J]. Ecology, 2021, 102(7):e03337.DOI:10.1002/ecy.3337.
[39]	贾宁, 唐研耀, 曾燕如, 等. 植物无融合生殖研究进展[J]. 生物技术通报, 2015, 31(12):15-24.
	JIA N, TANG Y Y, ZENG Y R, et al. Research progress on apomixis in plants[J]. Biotechnol Bull, 2015, 31(12):15-24.DOI:10.13560/j.cnki.biotech.bull.1985.2015.12.003.
[40]	XIAO H W, LUO H L, LIU N N, et al. High fruit setting rate without male participation:a case study of obligate apomixis in Rhomboda tokioi (Orchidaceae)[J]. Flora, 2021, 283:151920.DOI:10.1016/j.flora.2021.151920.
[41]	DART S, ECKERT C G. Experimental manipulation of flowers to determine the functional modes and fitness consequences of self-fertilization: unexpected outcome reveals key assumptions[J]. Funct Ecol, 2013, 27(2):362-373.DOI:10.1111/1365-2435.12055.
[42]	GOODWILLIE C, PARTIS K, WEBER J. Transient self-incompatibility confers delayed selfing in Leptosiphon jepsonii (Polemoniaceae)[J]. Int J Plant Sci, 2004, 165(3):387-394.DOI:10.1086/382805.
[43]	DOLE J A. Reproductive assurance mechanisms in three taxa of the Mimulus guttatus complex (Scrophulariaceae)[J]. Am J Bot, 1992, 79(6):650-659.DOI:10.1002/j.1537-2197.1992.tb14607.x.
[44]	DOLE J A. Role of Corolla abscission in delayed self-pollination of Mimulus guttatus (Scrophulariaceae)[J]. Am J Bot, 1990, 77(11):1505-1507.DOI:10.2307/2444762.
[45]	LECLERC-POTVIN C, RITLAND K. Modes of self-fertilization in Mimulus guttatus (Scrophulariaceae):a field experiment[J]. Am J Bot, 1994, 81(2):199-205.DOI:10.2307/2445634.
[46]	CUTTER A D. Reproductive transitions in plants and animals:selfing syndrome,sexual selection and speciation[J]. New Phytol, 2019, 224(3):1080-1094.DOI:10.1111/nph.16075.
[47]	MIYAJIMA D. Seed producing system in Portulaca oleraceae L[J]. Asian J Plant Sci, 2006, 5(2):226.DOI:10.3923/ajps.2006.226.232.
[48]	REN Y Q, XU Y P, ZHANG T, et al. Growth discrepancy between filament and style facilitates self‐fertilization in Brandisia hancei (Paulowniaceae)[J]. Plant Species Biol, 2016, 31:153-158.DOI:10.1111/1442-1984.12099.
[49]	BROWN K E, KELLY J K. Severe inbreeding depression is predicted by the rare allele load in Mimulus guttatus[J]. Evolution, 2020, 74(3):587-596.DOI:10.1111/evo.13876.
[50]	RODDY A B, MARTÍNEZ-PEREZ C, TEIXIDO A L, et al. Towards the flower economics spectrum[J]. New Phytol, 2021, 229(2):665-672.DOI:10.1111/nph.16823.
[51]	OROZCO-IBARROLA O A, FLORES-HERNÁNDEZ P S, VICTORIANO-ROMERO E, et al. Are breeding system and florivory associated with the abundance of Tillandsia species (Bromeliaceae)?[J]. Bot J Linn Soc, 2015, 177(1):50-65.DOI:10.1111/boj.12225.
[52]	肖汉文, 黄艳波, 王琦, 等. 高山物种栗色鼠尾草(Salvia castanea Diels)访花昆虫多样性与传粉行为变化[J]. 生态学报, 2022, 42(5):1841-1853.
	XIAO H W, HUANG Y B, WANG Q, et al. Diversity of visiting insects and changes of pollinator behavior in alpine species Salvia castanea Diels (Lamiaceae)[J]. Acta Ecol Sin, 2022, 42(5):1841-1853.DOI:10.5846/stxb202101070071.
[53]	VOILLEMOT M, ENCINAS-VISO F, PANNELL J R. Rapid loss of self-incompatibility in experimental populations of the perennial outcrossing plant Linaria cavanillesii[J]. Evolution, 2019, 73(5):913-926.DOI:10.1111/evo.13721.
[54]	BROZ A K, DAM A S V, TOVAR-MÉNDEZ A, et al. Spread of self-compatibility constrained by an intrapopulation crossing barrier[J]. New Phytol, 2021, 231(2):878-891.DOI:10.1111/nph.17400.
[55]	SUETSUGU K. Delayed autonomous self-pollination in two Japanese varieties of Epipactis helleborine (Orchidaceae)[J]. Bot J Linn Soc, 2013, 173(4):733-743.DOI:10.1111/boj.12111.
[56]	IRWIN J A, ASHTON P A, BRETAGNOLLE F, et al. The long and the short of it:long-styled florets are associated with higher outcrossing rate in Senecio vulgaris and result from delayed self-pollen germination[J]. Plant Ecol Divers, 2016, 9(2):159-165.DOI:10.1080/17550874.2016.1181116.
[57]	GARCÍA-DORADO A. An explicit model for the inbreeding load in the evolutionary analysis of selfing[J]. Evolution, 2017, 71(5):1381-1389.DOI:10.1111/evo.13231.

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