Abstract
Floral organ movements that ensure autonomous selfing are likely to occur in species that grow in habitats with pollinator scarcity and/or an unpredictable environment. Stamen curvature and temporal flower closure are two important floral behaviors that can influence plant pollination mode and reproductive success. However, both behaviors are rarely reported within a species, and little is known about how these two movements of floral organs ensure reproductive success in an unpredictable early spring environment with few pollinators. The aim of this study was to assess whether stamen curvature and temporal flower closure ensure successful reproduction of Leontice incerta in its cold desert habitat. Flowering phenology, floral traits, stamen curvature patterns and flower visitors were surveyed. The breeding system, capacity and timing for autonomous selfing were estimated by pollination manipulations. The timing of floral opening and closure, and benefits of temporal flower closure were determined. We found that flowering of L. incerta began in late March to early April in two populations in two years, and the yellow flowers had neither nectar nor scent. Floral visitation occurred very rarely, but bees (Colletes sp.) were potential pollinators. Fruit and seed set of open and bagged flowers did not differ significantly from that of self-pollinated or cross-pollinated flowers. However, removal of stamens significantly decreased seed set. Self-pollination occurs when the stamens curve and anthers touch the stigma autonomously, suggesting autonomous selfing assurance of seed production in this self-compatible species. Both fruit and seed set of flowers that were prevented from closing were significantly lower than those of control flowers and closed flowers treated with simulated rain treatment. Therefore, stamen curvature and temporal floral closure can ensure successful sexual reproduction of L. incerta in early spring in the cold desert, where lack of pollinators otherwise may lead to pollination failure.
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References
Abdusalam A, Tan DY (2014) Contribution of temporal floral closure to reproductive success of the spring-flowering, Tulipa iliensis. J Syst Evol 52:186–194. https://doi.org/10.1111/jse.12036
Andrews FM (1929) The effect of temperature on flowers. Plant Physiol 4:281–284. https://doi.org/10.1104/pp.4.2.281
Arroyo MTK, Dudley LS, Jespersen G, Pacheco DA, Cavieres LA (2013) Temperature-driven flower longevity in a high-alpine species of Oxalis influences reproductive assurance. New Phytol 200:1260–1268. https://doi.org/10.1111/nph.12443
Baker HG (1955) Self-compatibility and establishment after ‘“longdistance”’ dispersal. Evolution 9:347–348. https://doi.org/10.1111/j.1558-5646.1955.tb01544.x
Burns KC (2014) Are there general patterns in plant defense against megaherbivores? Biol J Linn Soc 111:38–48. https://doi.org/10.1111/bij.12181
Bynum MR, Smith WK (2001) Floral movement in response to thunderstorms improve reproductive effort in the alpine species Gentiana algida (Gentianaceae). Am J Bot 88:1088–1095. https://doi.org/10.2307/2657092
Castillo RA, Cordero C, Domínguez CA (2002) Are reward polymorphisms subject to frequency-and density-dependent selection? Evidence from a monoecious species pollinated by deceit. J Evol Biol 15:544–552. https://doi.org/10.1046/j.1420-9101.2002.00425.x
Chen LJ, Liu KW, Xiao XJ, Tsai WC, Hsiao YY, Huang J, Liu ZJ (2012) The anther steps onto the stigma for self-fertilization in a slipper orchid. PLoS ONE 7:e37478. https://doi.org/10.1371/journal.pone.0037478
Christopher DA, Karron JD, Semski WR, Smallwood PA, Trapnell DW, Mitchell RJ (2021) Selfing rates vary with floral display, pollinator visitation and plant density in natural populations of Mimulus ringens. J Evol Biol 34:803–815. https://doi.org/10.1111/jeb.13781
Cortés-Flores KB, Hernández-Esquivel A, González-Rodríguez G, Ibarra-Manríquez G (2017) Flowering phenology, growth forms, and pollination syndromes in tropical dry forest species: influence of phylogeny and abiotic factors. Am J Bot 104:39–49. https://doi.org/10.3732/ajb.1600305
Dafni A (1996) Autumnal and winter pollination adaptation under Mediterranean conditions. Bocconea 5:171–181
Dafni A, Kevan PG, Husband BC (2005) Practical pollination biology. Enviroquest, Cambridge
Darwin C (1876) The effects of cross and self-fertilization in the vegetable kingdom. John Murray Press, London
Davis SL, Delph LF (2005) Prior selfing and gynomonoecy in Silene noctiflora L. (Caryophyllaceae): opportunities for enhanced outcrossing and reproductive assurance. Int J Plant Sci 166:475–480. https://doi.org/10.1086/428630
Dole JA (1990) Role of corolla abscission in delayed self-pollination of Mimulus guttatus (Scrophulariaceae). Am J Bot 77:1505–1507
Etcheverry AV, Protomastro JJ, Westerkamp C (2003) Delayed autonomous self-pollination in the colonizer Crotalaria micans (Fabaceae: Papilionoideae): structural and functional aspects. Plant Syst Evol 239:15–28
Evans M, Hearn DJ, Theiss KE, Cranston K, Holsinger KE, Donoghue MJ (2011) Extreme environments select for reproductive assurance: evidence from evening primroses (Oenothera). New Phytol 191:555–563. https://doi.org/10.1111/j.1469-8137.2011.03697.x
Fetscher AE, Kohn JR (1999) Stigma behavior in Mimulus aurantiacus (Scrophulariaceae). Am J Bot 86:1130–1135. https://doi.org/10.2307/2656976
Freitas L, Sazima M (2009) Floral biology and mechanisms of spontaneous self-pollination in five neotropical species of Gentianaceae. Bot J Linn Soc 160:357–368. https://doi.org/10.1111/j.1095-8339.2009.00989.x
Gutterman Y (2002) Survival strategies of annual desert plants. Springer, Berlin
Hafdahl CE, Craig TP (2014) Flowering phenology in Solidago altissima: adaptive strategies against temporal variation in temperature. J Plant Interact 9: 122–127. https://doi.org/10.1080/17429145.2013.777478
Harder LD, Barrett SCH (1996). Pollen dispersal and mating patterns in animal-pollinated plants. In: Lloyd DG, Barrett SCH (eds) Floral biology: studies on floral evolution in animal-pollinated plants, Chapman & Hall, New York, pp 140–190.
Harder LD, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature 373:512–515. https://doi.org/10.1038/373512a0
He YP, Duan YW, Liu JQ, Smith WK (2006) Floral closure in response to temperature and pollination in Gentiana straminea Maxim. (Gentianaceae), an alpine perennial in the Qinghai Tibetan Plateau. Plant Syst Evol 256:17–33
Huang SQ, Takahashi Y, Dafni A (2002) Why does the flower stalk of Pulsatilla cernua (Ranunculaceae) bend during anthesis? Am J Bot 89:1599–1603. https://doi.org/10.3732/ajb.89.10.1599
Ichimura K, Suto K (1998) Environmental factors controlling flower opening and closing in a portulaca hybrid. Ann Bot 82:67–70. https://doi.org/10.1006/anbo.1998.0642
Jain SK, Allard RW (1960) Population studies in predominantly self-pollinated species. I. Evidence for heterozygote advantage in a closed population of barley. Proc Natl Acad Sci USA 46:1371–1377. https://doi.org/10.1073/pnas.46.10.1371
Juncosa AM, Webster BD (1989) Pollination in Lupinus nanus (Leguminosae). Am J Bot 76:59–66
Jürgens A, Witt T (2014) Pollen-ovule ratios and flower visitors of day-flowering and night-flowering Conophytum (Aizoaceae) species in south Africa. J Arid Environ 109:44–53. https://doi.org/10.1016/j.jaridenv.2014.05.004
Kalisz S, Vogler D, Fails B, Finer M, Shepard E, Herman T, Gonzales R (1999) The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae). Am J Bot 86:1239–1247. https://doi.org/10.2307/2656771
Li JK, Huang SQ (2009) Flower thermoregulation facilitates fertilization in Asian sacred lotus. Ann Bot 103:1159–1163. https://doi.org/10.1093/aob/mcp051
Li Q, Ruan CJ, Teixeira da Silva JA, Wang XY (2012) Floral morphology and mating system of Alcea rosea (Malvaceae). Plant Ecol Evol 145:176–184. https://doi.org/10.5091/plecevo.2012.651
Liu KW, Liu ZJ, Huang LQ, Li LQ, Chen LJ, Tang GD (2006) Self-fertilization strategy in an orchid. Nature 441:945–946
Liu FY, Gao CJ, Chen M, Tang GY, Sun YY, Kun Li (2021) The impacts of flowering phenology on the reproductive success of the narrow endemic Nouelia insignis Franch. (Asteraceae). Ecol Evol 11:9396–9409. https://doi.org/10.1002/ece3.7747
Lloyd DG (1992) Self-fertilization and cross-fertilization in plants. II. The selection of self-fertilization. Int J Plant Sci 153:370–380. https://doi.org/10.1086/297041
Lloyd DG, Schoen DJ (1992) Self- and cross-fertilization in plants. I. Functional dimensions. Int J Plant Sci 153:358–369. https://doi.org/10.1086/297040
Lyon DL (1992) Bee pollination of facultatively xenogamous Sanguinaria canadensis L. Bull Torrey Bot Club 119:368–375. https://doi.org/10.1093/aob/mcp051
Mallick SA (2001) Facultative dichogamy and reproductive assurance in partially protandrous plants. Oikos 95:533–535. https://doi.org/10.1034/j.1600-0706.2001.950318.x
Mamut J, Li B, Tan DY (2014) Protogyny and delayed autonomous self-pollination in the desert herb Zygophyllum macropterum (Zygophyllaceae). J Syst Evol 52:75–83. https://doi.org/10.1111/jse.12029
Mamut J, Zhang CY, Tan DY, Baskin CC, Baskin JM (2020) Versatility in the timing of seed germination of the cold desert herbaceous perennial Leontice incerta (Berberidaceae). Seed Sci Res 30:37–44. https://doi.org/10.1017/s0960258520000100
Mao YY, Huang SQ (2009) Pollen resistance to water in 80 angiosperm species: flower structures protect rain susceptible pollen. New Phytol 183:892–899. https://doi.org/10.1111/j.1469-8137.2009.02925.x
Motten AF (1986) Pollination ecology of the spring wildflower community of a temperate deciduous forest. Ecol Monogr 56:21–42
Prokop P, Neupauerová D (2014) Flower closure in the field bindweed (Convolvulus arvensis): a field test of the pollination hypothesis. Turk J Bot 38:877–882. https://doi.org/10.3906/bot-1310-57
Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214. https://doi.org/10.1146/annurev.es.16.110185.001143
Ren MX, Tang JU (2012) Up and down: stamen movements in Ruta graveolens (Rutaceae) enhance both outcrossing and delayed selfing. Ann Bot 110:1017–1025. https://doi.org/10.1093/aob/mcs181
Ruan CJ, da Silva JAT (2011) Adaptive significance of floral movement. Crit Rev Plant Sci 30:293–328. https://doi.org/10.1080/07352689.2011.587715
Ruan CJ, Qin P, He ZX (2004) Delayed autonomous selfing in Kosteletzkya virginica (Malvaceae). S Afr J of Bot 70:640–645. https://doi.org/10.1016/S0254-6299(15)30204-0
Ruan CJ, Mopper S, Silva J, Qin P, Zhang QX, Shan Y (2009) Context-dependent style curvature in Kosteletzkya virginica (Malvaceae) offers reproductive assurance under unpredictable pollinator environments. Plant Syst Evol 277:207–215. https://doi.org/10.1007/s00606-008-0127-7
Ruan CJ, Teixeira da Silva JA, Qin P (2010) Style curvature and its adaptive significance in the Malvaceae. Plant Syst Evol 288:13–23. https://doi.org/10.1007/s00606-010-0305-2
Saunders NE, Sedonia DS (2006) Reproductive biology and pollination ecology of the rare Yellowstone Park endemic Abronia ammophila (Nyctaginaceae). Plant Spec Biol 21:75–84. https://doi.org/10.1111/j.1442-1984.2006.00153.x
Schemske DW (1978) Sexual reproduction in an Illinois population of Sanguinaria canadensis L. Am Midl Nat 2:261–268
Schlessman MA (1986) Floral protogyny, self-compatibility and the pollination of Ourisia macrocarpa (Scrophulariaceae). New Zeal J Bot 24:651–656. https://doi.org/10.1080/0028825X.1986.10409948
Shi X, Wang JC, Zhang DY, Gaskin JF, Pan BR (2010) Pollination ecology of the rare desert species Eremosparton songoricum (Fabaceae). Aust J Bot 58:35–41. https://doi.org/10.1071/BT09172
Shivanna KR (2015) Reproductive assurance through autogamous self-pollination across diverse sexual and breeding systems. Curr Sci 109:1255–1263
Smith GF, Chesselet P, van Jaarsveld EJ, Hartmann H, Hammer S, van Wyk BE, Burgoyne P, Klak C, Kurzweil H (1998) Mesembs of the world. Briza Publications, Pretoria
Song B, Zhang ZQ, Stöcklin J, Yang Y, Niu Y, Chen JG, Sun H (2013) Multifunctional bracts enhance plant fitness during flowering and seed development in Rheum nobile (Polygonaceae), a giant herb endemic to the high Himalayas. Oecologia 172:359–370. https://doi.org/10.1007/s00442-012-2518-2
Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York
Stirton CH (1983) Nocturnal petal movements in Asteraceae. Bothalia 14:1003–1006
Sun SG, Guo YH, Gituru RW, Huang SQ (2005) Corolla wilting facilitates delayed autonomous self-pollination in Pedicularis dunniana (Orobanchaceae). Plant Syst Evol 251:229–237. https://doi.org/10.1007/s00606-004-0260-x
Sun JF, Gong YB, Renner SS, Huang SQ (2008) Multifunctional bracts in the dove tree Davidia involucrate (Nyssaceae: Cornales): rain protection and pollinator attraction. Am Nat 171:119–124. https://doi.org/10.1086/523953
Tagawa K, Watanabe M, Yahara T (2018) A sensitive flower: mechanical stimulation induces rapid flower closure in Drosera spp. (Droseraceae). Plant Spec Biol 33:153–157. https://doi.org/10.1111/1442-1984.12203
Tao Y, Qiu D, Gong YM, Liu HL, Zhang J, Yin BF, Lu HY,·Zhou XB, Zhang YM, (2022) Leaf-root-soil N: P stoichiometry of ephemeral plants in a temperate desert in Central Asia. J Plant Res 135:55–67. https://doi.org/10.1007/s10265-021-01355-8
Taylor PE, Card G, House DMH, Flagan RC (2006) High-speed pollen release in the white mulberry tree Morus alba L. Sex. Plant Reprod 19:19–24
van Doorn WG, Kamdee C (2014) Flower opening and closure: an update. J Exp Bot 65:5749–5757
van Doorn WG, van Meeteren U (2003) Flower opening and closure: a review. J Exp Bot 54:1801–1812. https://doi.org/10.1093/jxb/erg213
Vaughton G, Ramsey M (2010) Pollinator-mediated selfing erodes the flexibility of the best of both worlds mating strategy in Bulbine vagans. Funct Ecol 24:374–382. https://doi.org/10.1111/j.1365-2435.2009.01648.x
Verma S, Magotra R, Koul AK (2004) Stylar movement avoids self-pollination and promotes cross-pollination in Eremurus himalaicus. Curr Sci 87:872–873
von Hase A, Cowling RM, Ellis AG (2006) Petal movement in cape wildflowers protects pollen from exposure to moisture. Plant Ecol 184:75–87. https://doi.org/10.1007/s11258-005-9053-8
Wang SH (2008) Soil and water conservation program of Shawan county. Soil Water Conser China 11:44–45 ([in Chinese])
Wang ZC (2013) Pollutant characteristics of ambient air quality in Dushanzi district Karamay. North Hortic 25:72–75 ([in Chinese with English abstract])
Wang Y, Meng LH, Yang YP, Duan YW (2010) Change in floral orientation in Anisodus luridus (Solanaceae) protects pollen grains and facilitates development of fertilized ovules. Am J Bot 97:1618–1624. https://doi.org/10.3732/ajb.1000010
Willmer PG (2011) Pollination and floral ecology. Princeton University Press, Princeton, New Jersey (ISBN: 9780691128610)
Xiong YZ, Fang Q, Huang SQ (2013) Pollinator scarcity drives the shift to delayed selfing in Himalayan mayapple Podophyllum hexandrum (Berberidaceae). AoB Plants 5, plt037. https://doi.org/10.1093/aobpla/plt037
Xu HX, Zhang X, Wang SM, Yan P, Du JZ (2008) Genetic diversity of Achnatherum splendens. Agr Sci Technol 9:21–23 ([in Chinese with English abstract])
Yang CF, Guo YH, Gituru RW, Sun SG (2002) Variation in stigma morphology-How does it contribute to pollination adaptation in Pedicularis (Orobanchaceae)? Plant Syst Evol 236:89–98. https://doi.org/10.1007/s00606-002-0223-z
Yang LM, Shi YG, Tang H (2010) Characteristics of atmospheric circulation and water vapor for spring precipitation anomaly in Xinjiang. Plateau Meteorol 29:1464–1473 ((in Chinese with English abstract))
Ying JS, Boufford DE, Brach AR (2001) Berberidaceae. In Wu ZY, Raven PH (eds) Flora of China. Science Press, Beijing; Missouri Botanical Garden Press, St. Louis.
Zufall RA, Rausher MD (2004) Genetic changes associated with floral adaptation restrict future evolutionary potential. Nature 428:847–850. https://doi.org/10.1038/nature02489
Acknowledgements
We thank Professors Carol C. Baskin and Jerry M. Baskin (University of Kentucky, Lexington, USA) for revision of the manuscript, YB Gong (Wuhan University) for providing very valuable suggestions and HZ Ma and ZY Wang for help in the field. This study was supported by the National Natural Science Foundation of China (31760060, 31960053 and U1603231).
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DYT and JM designed the study; JM, DHH and JQ performed experiments; JM analyzed the data; All authors wrote the manuscript.
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Mamut, J., Huang, DH., Qiu, J. et al. Stamen curvature and temporal flower closure assure reproductive success in an early-spring-flowering perennial in the cold desert of Middle Asia. J Plant Res 136, 33–45 (2023). https://doi.org/10.1007/s10265-022-01428-2
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DOI: https://doi.org/10.1007/s10265-022-01428-2