A review of delayed autonomous selfing in flowering plants

XIAO Hanwen, LIU Qingshan, TIAN Runan

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2022, Vol. 46 ›› Issue (6) : 233-239.

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南京林业大学学报（自然科学版）
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JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2022, Vol. 46 ›› Issue (6) : 233-239. DOI: 10.12302/j.issn.1000-2006.2022008031

A review of delayed autonomous selfing in flowering plants

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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

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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 https://doi.org/10.12302/j.issn.1000-2006.2022008031

References

List( Publishing order | Descend order by publishing year | Descend order by cited within ) Chart analysis
[1]
BARRETT S C H. The evolution of plant sexual diversity[J]. Nat Rev Genet, 2002, 3(4):274-284.DOI:10.1038/nrg776.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [3]
[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.
Cited in this article [3]
[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.
Cited in this article [3]
[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.
Cited in this article [3]
[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.
Cited in this article [6]
[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.
Cited in this article [11]
[9]
ASHMAN T L, SCHOEN D J. How long should flowers live?[J]. Nature, 1994, 371(6500):788-791.DOI:10.1038/371788a0.
Cited in this article [3]
[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.
Cited in this article [6]
[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.
Cited in this article [3]
[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.
Cited in this article [10]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [2]
[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.
Cited in this article [1]
[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.
Cited in this article [3]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [2]
[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.
Cited in this article [2]
[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.
Cited in this article [2]
[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.
Cited in this article [1]
[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.
Cited in this article [2]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [4]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [2]
[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.
Cited in this article [1]
[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.
Cited in this article [2]
[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.
Cited in this article [2]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [2]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]
[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.
Cited in this article [1]

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