The Classification and Functional Significance of Staminodes in Angiosperms

doi:10.7677/ynzwyj201515060

Abstract

Abstract:

All staminodes in an androecium fail to produce viable pollen grains and cannot contribute directly to male fitness. Staminodes are identified in the flowers of approximately 54% of known genera representing >32% of all angiosperm families. The functional morphology and biochemistry of staminodes differs significantly from stamens with fertile anthers. In the absence of sperm production, some staminodes evolved novel adaptations contributing to the reproductive success of their flowers. We subdivided these staminodes into eight functional types: 1) Staminodes offering visual/olfactory cues; 2) Staminodes offering edible/inedible rewards; 3) Staminodes that deceive pollinators with false rewards; 4) Staminodes facilitating or directing the movements of pollinators in flowers;5) Stami
nodes that facilitate stigma movement; 6) Staminodes functioning as secondary pollen presenters; 7) Staminodes that protect other floral organs; 8) Staminodes that prevent mechanical selfpollination (autogamy). As a component within a flower, the majority of staminodes function as promoters of reproductive success by interacting directly with the pollinator to increase pollination efficiency (both pollen dispersal and deposition). Therefore, it is not surprising that one staminode may have more than one function over the flower′s lifespan and is closely associated with the size, abundance, behavior and taxonomic diversity of pollinators, floral predators and thieves. To correctly evaluate the function of staminodes, multidisciplinary approach using a range of protocols, equipment and materials is suggested. This approach allows us to compare the roles different staminodes play in the reproductive success of both closely and distantly related angiosperms, then uncover their evolutionary significance in angiosperm diversification.

Key words: Staminode, Reproductive success, Functional divergence, Evolution, Plant-pollinator interaction

摘要：

退化雄蕊是指没有花药或花药不可育的雄蕊，发现于被子植物325%的科以及544%的属中，它们在形态和生化组成上都与可育雄蕊有着显著区别。虽然丢失了产生可育花粉的能力、无法发挥雄性繁殖功能，某些退化雄蕊在进化过程中重新获得了一些有助于植物繁殖成功的新功能。本文将这些具有功能的退化雄蕊细分为8类：（1）信号型；（2）报酬型；（3）欺骗传粉型；（4）辅助传粉昆虫在花内活动；（5）辅助授粉；（6）协助花粉二次呈现；（7）保护其他花结构；（8）避免自交。退化雄蕊作为花结构的一部分，其功能集中于促进植物的繁殖成功，主要通过与传粉昆虫的相互作用来提高传粉效率。此外，某些植物的退化雄蕊也可能同时具有多种功能，并且其功能的强弱与传粉者的种类、行为、大小和频率相关。正确评估退化雄蕊对植物繁殖成功的影响，需要多学科手段来系统的研究，以便能更加深入的理解不同近缘关系的物种间退化雄蕊功能的差异，揭示退化雄蕊在被子植物系统进化中的意义。

关键词: 退化雄蕊, 传粉, 功能分化, 进化, 植物-传粉者互作

CLC Number:

Q 944，Q 948

CHEN Shan-, REN Zong-Xin-, WANG Hong-, Wu Ding. The Classification and Functional Significance of Staminodes in Angiosperms[J]. Plant Diversity, 2015, 37(06): 683-692.

陈珊1、2, 任宗昕2, 王红2, 吴丁3. 被子植物退化雄蕊的功能类型及其意义[J]. Plant Diversity, 2015, 37(06): 683-692.

References

Armstrong JE, Irvine AK, 1990. Functions of staminodia in the beetlepollinated flowers of Eupomatia laurina［J］. Biotropica, 22 (4): 429—431
Argue CL, 2005. Pollination biology of the clustered lady slipper［J］. Tremontia, 33: 23—28
Atwood JT, 1985. Pollination of Paphiopedilum rothschildianum: broodsite deception［J］. National Geographic Research, 1: 247—254
Bziger H, 1996. The mesmerizing wart: the pollination strategy of epiphytic lady slipper orchid Paphiopedilum villosum (Lindl.) Stein (Orchidaceae) ［J］. Botanical Journal of the Linnean SocietyVolume, 121 (1): 59—90
Bnziger H, Sun HQ, Luo YB, 2005. Pollination of a slippery lady slipper orchid in southwest China: Cypripedium guttatum (Orchidaceae) ［J］. Botanical Journal of the Linnean Society, 148 (3): 251—264
Beach JH, 1982. Beetle pollination of Cyclanthus bipartitus (Cyclanthaceae) ［J］. American Journal of Botany, 69 (7): 1074—1081
Brayshaw CT, 1989. Buttercups, waterlilies and their relatives in British columbia［J］. Royal British Columbia Museum Memoir, 1: 1—253
ClaenBockhoff R, Speck T, Tweraser E et al., 2004. The staminal lever mechanism in Salvia L. (Lamiaceae): A key innovation for adaptive radiation?［J］. Organisms, Diversity and Evolution, 4: 189—205
ClaenBockhoff R, Wester P, Tweraser E, 2003. The staminal lever mechanism in Salvia L. (Lamiaceae): a review［J］. Plant Biology, 5: 33—41
ClaenBockhoff R, Heller A, 2008. Floral synorganization and secondary pollen presentation in four Marantaceae from Costa［J］. International Journal of Plant Sciences, 169 (6): 745—760
Cronquist A, 1981. An Integrated System of Classification of Flowering Plants［M］. New York, USA: Columbia University Press
Darwin C, 1877. The Different Forms of Flowers on Plants of the Same Species［M］. London: John Murray
Daumann E, 1935.trber die Bestaubungsokologie der ParnassiaBliite. II. Ein weiterer Beitrag zur experimentellen Bliitenforschung［J］. Jahrbücher für Wissenschaftbiche Botanik, 81: 705—717
Decraene LPR, Smets E, 1991. Androecium and floral nectaries of Harungana madagascariensis (Clusiaceae) ［J］. Plant Systematics and Evolution, 178: 179—194
Decraene LPR, Smets E, 2001. Staminodes: their morphological and evolutionary significance［J］. Botanical Review, 67 (3): 351—402
Dieringer G, Cabrera RL, 2002. The interaction between pollinator size and the bristle staminode of Penstemon digitalis (Scrophulariaceae) ［J］. American Journal of Botany, 89 (6): 991—997
Dickison WC, Weitzman AL, 1998. Floral morphology and anatomy of Bonnetiaceae［J］.Journal of the Torrey Botanical Society, 125: 268—286
Duan YA (段友爱), Li QJ ( 李庆军), 2008. The pollination biology of Phrynium oliganthum (Marantaceae) ［J］. Journal of Systematics and Evolution (植物分类学报), 46 (4): 545—553
Dulberger R, 1981. The floral biology of Cassia didymobotrya and Cauriculata (Caesalpiniaceae) ［J］. American Journal of Botany, 68 (10): 1350—1360
EdensMeier R, Westhus E, Bernhardt P, 2013. Floral biology of largeflowered Thelymitra species (Orchidaceae) and their hybrids in Western Australia［J］. Telopea, 15: 165—183
Endress PK, 1984. The role of inner staminodes in the floral display of some relic Magnoliales［J］. Plant Systematics and Evolution, 146: 269—282
Endress PK, 1994. Diversity and Evolutionary Biology of Tropical Flowers［M］. Cambridge, UK: Cambridge University Press
Faden RB, 1992. Floral attraction and floral hairs in the Commelinaceae［J］. Annals of the Missouri Botanical Garden, 79 (1): 46—52
Faegri K, Der LPV, 1979. The Principles of Pollination Ecology, 3rd revised ed［M］. Oxford, UK: Pergamon Press
Freitas BM, Paxton RJ, 1996. The role of wind and insects in cashew (Anacardium occidentale) pollination in NE Brazil［J］. Journal of Agricultural Science, 126: 319—326
Glinos E, Cocucci AA, 2011. Pollination biology of Canna indica (Cannaceae) with particular reference to the functional morphology of the style［J］. Plant Systematics and Evolution, 291: 49—58
Guimaraes E, Luiz CDS, Di Stasi LC et al., 2008. Pollination biology of Jacaranda oxyphylla with an emphasis on staminode function［J］. Annals of Botany, 102: 699—711
Hawk JL, Tepedino VJ, 2007. The effect of staminode removalon female reproductive success in a wyoming population of the endangered blowout penstemon, Penstemon haydenii (Scrophulariaceae) ［J］. Madroo, 54 (1): 22—26
Hemsley WB, 1903. On the genus Corynocarpus, Forst., with descriptions of two new species［J］. Annals of Botany, 17 (4): 743—760
Heywood VH, 1985. Flowering Plants of the World, 2nd ed ［M］. Prentice Hall, New Jersey, USA: Englewood Cliffs
Hofmann U, 1994. Flower Morphology and Ontogeny［M］. Caryophyllales: Evolution and systematics. Berlin, SpringerVerlag, 123—166
Holm E, 1978. Some unusual pollination mechanisms in western Australian wildflowers［J］. Western Australian Naturalist, 14: 60—62
Howell GJ, Slater AT, Knox RB, 1993. Secondary pollen presentation in angiosperms and its biological significance［J］. Australian Journal of Botany, 41: 417—438
Kirchoff BK, 1983. Allometric growth of the flowers in five genera of the Marantaceae and in Canna (Cannaceae) ［J］. Botanical Gazette, 144 (1): 110—118
Kirchoff BK, 1991. Homeosis in the flowers of the Zingiberales［J］. American Journal of Botany, 78 (6): 833—837
Ley AC, ClaenBockhoff R, 2009. Pollination syndromes in African Marantaceae［J］. Annals of Botany, 104 (1): 41—56
Ley AC, ClaenBockhoff R, 2011. Evolution in African Marantaceae—Evidence from Phylogenetic, Ecological and Morphological Studies［J］. Systematic Botany, 36 (2): 277—290
Li P, Luo Y, Bernhardt P et al., 2008. Pollination of Cypripedium plectrochilum (Orchidaceae) by Lasioglossum spp. (Halictidae): The roles of generalist attractants versus restrictive floral architecture［J］. Plant Biology, 10: 220—230
Liao MZ (缪明志), Liu HF (刘焕芳), Kuang YF (匡延凤) et al., 2014. Floral vasculature anatomy of Canna glauca ‘Erebus’ (Cannaceae) ［J］. Journal of Tropical and Subtropical Botany (热带亚热带植物学报), 22 (4): 344—350
Link DA, 1991. The floral nectaries of geraniales. III. Lepidobotryaceae. Léonard［J］. Bulletin du Jardin Botanique National de Belgique/Bulletin van de National Plantentuin van Belgi, 61 (3/4): 347—354
Luo ZL (罗中莱), Zhang DX (张奠湘), 2005. A review of heteranthery in flowering plants［J］. Journal of Tropical and Subtropical Botany (热带亚热带植物学报), 13 (6): 536—542
Lunau, 2006. Stamens and mimic stamens as components of floral colour patterns［J］. Botanische Jahrbücher, 127 (1): 13—41
Mori SA, Prance GT, BoltenAB, 1978. Additional notes on the floral biology of neotropical Lecythidaceae［J］. Brittonia, 30: 113—130
Müller F, 1883. Two kinds of stamens with different function in the same flower［J］. Nature, Feb (15): 364—365
Nilsson LA, 1979. Anthecological studies of the Lady’sslipper, Cypripedium calceolus (Orchidaceae) ［J］. Botaniska Notiser, 132: 329—347
Pischtschan E, Ley AC, ClaenBockhoff R, 2010. Ontogenetic and phylogenetic diversification of the hooded staminode in Marantaceae［J］. Taxon, 59 (4): 1111—1125
Plitmann U, Raven PH, Breedlove DE, 1973. The systematics of Lopezieae (Onagraceae) ［J］. Annals of the Missouri Botanical Garden, 60: 478—563
Prance GT, 1976. The pollination and androphore structure of some amazonian Lecythidaceae［J］. Biotropica, 8 (4): 235—241
Ren ZX (任宗昕), Wang H (王红), Luo YB (罗毅波), 2012. Deceptive pollination of orchids［J］. Biodiversity Science (生物多样性), 20: 270—279
Rickson FR, 1979. Ultrastructural development of the beetle food tissue of Calycanthus flowers［J］. American Journal of Botany, 66 (1): 80—86
Sandvik SM, Totland O, 2003.Quantitative importance of staminodes for female reproductive success in Parnassia palustris under contrasting environmental conditions［J］. Canadian Journal of Botany, 81: 49—56
Shi J, Luo YB, Bernhardt P et al., 2009. Pollination by deceit in Paphiopedilum barbigerum (Orchidaceae): a staminode exploits the innate colourpreferences of hoverflies (Syrphidae) ［J］. Plant Biology, 11: 17—28
Straw RM, 1956. Adaptive morphology of the Penstemon flower［J］. Phytomorphology, 6: 112—119
Sutherland D, 2006.The impact of variation in‘false’food signalling on the pollination success of Phacelia campanularia and Parnassia palustris［D］. Aberdeen: University of Aberdeen
Tian DJ (田军东), Shi TS (史团省), Zhu SX (朱世新) et al., 2007. Preliminary studyand observation on the insectcatching behaviour of Thalia dealbata Fraser［J］. World SciTech R & D (世界科技研究与发展), 29 (6): 62—65
Vogel S, 1978. Evolutionary shifts from reward to deception in pollen flowers［A］// Richards AJ ed., The Pollination of Flowers by Insects. Linnean Society Symposium, Series 6［M］. London: Academic Press, 89—96
Vogt CA, 1990. Pollination in Cypripedium reginae (Orchidaceae) ［J］. Lindleyana, 5: 145—150
WalkerLarsen J, Harder LD, 2000. The evolution of staminode in angiosperms［J］. American Journal of Botany, 87 (10): 1367—1384
WalkerLarsen J, Harder LD, 2001. Vestigial organs as opportunities for functional innovation: the example of the Penstemon staminode［J］. Evolution, 55 (3): 477—487
Weberling F, 1989. Morphology of Flowers and Inflorescences［M］. London: Cambridge University Press, UK
Yeo PF, 1992. Secondary Pollen Presentation: Form, Function and Evolution［M］. New York: SpringerVerlag, USA
Zhang B (张勃), Sun S (孙杉), Zhang ZQ (张志强) et al., 2010. A review of the evolutionary and ecological significance of leverlike stamens［J］. Chinese Journal of Plant Ecology (植物生态学报), 34 (1): 89—99
Zhang B (张勃), Sun S (孙杉), Fang QE (方强恩) et al.,2012. Evolutionary response of staminal lever mechanism of different species in Salvia to spatial variation in pollinators［J］. Chinese Journal of Plant Ecology (植物生态学报), 36 (7): 681—689
Zhang C (张婵), Cha SQ (查绍琴), Yang YP (杨永平) et al., 2012. Effects of the yellow barbs of the staminodes on reproductive success of Delphinium caeruleum (Ranunculaceae) ［J］. Biodiversity Science (生物多样性), 33 (1): 222—236

[1]	Fangdong Geng (耿方东), Miaoqing Liu (刘苗青), Luzhen Wang (王璐珍), Xuedong Zhang (张雪栋), Jiayu Ma (马佳雨), Hang Ye (叶航), Keith Woeste, Peng Zhao (赵鹏). Genomic introgression underlies environmental adaptation in three species of Chinese wingnuts, Pterocarya [J]. Plant Diversity, 2025, 47(03): 365-381.
[2]	Tao Zhang, Qiang Fang. Consistent spatial-temporal variations of stigmatic pollen load among co-flowering species across six sub-alpine meadows [J]. Plant Diversity, 2025, 47(03): 489-498.
[3]	Min-Fei Jin, Xiang-Hai Cai, Gao Chen. Seed dispersal by deception: A game between mimetic seeds and their bird dispersers [J]. Plant Diversity, 2025, 47(02): 169-177.
[4]	Haoxing Xie, Kaifeng Xing, Jun Zhou, Yao Zhao, Jian Zhang, Jun Rong. Single-nucleotide polymorphisms and copy number variations drive adaptive evolution to freezing stress in a subtropical evergreen broad-leaved tree: Hexaploid wild Camellia oleifera [J]. Plant Diversity, 2025, 47(02): 214-228.
[5]	Amos Kipkoech, Ke Li, Richard I. Milne, Oyetola Olusegun Oyebanji, Moses C. Wambulwa, Xiao-Gang Fu, Dennis A. Wakhungu, Zeng-Yuan Wu, Jie Liu. An integrative approach clarifies species delimitation and biogeographic history of Debregeasia (Urticaceae) [J]. Plant Diversity, 2025, 47(02): 229-243.
[6]	Hong Qian, Oriol Grau. Geographic patterns and ecological causes of phylogenetic structure in mosses along an elevational gradient in the central Himalaya [J]. Plant Diversity, 2025, 47(01): 98-105.
[7]	Xin Wang, Qing-Hong Feng, Zhi-Hua Zeng, Zhi-Qiang Zhang, Jie Cai, Gao Chen, De-Zhu Li, Hong Wang, Wei Zhou. Effects of mode of reproduction on genetic polymorphism and divergence in wild yams (Dioscoreaceae: Dioscorea) [J]. Plant Diversity, 2025, 47(01): 136-147.
[8]	Jin-Ru Zhong, Xiao-Fang Jin, Michael C. Orr, Xiao-Qing Li, Yong-Deng He, Sheng-Wei Wang, Qing-Feng Wang, Chun-Feng Yang, Zhong-Ming Ye. The ethics of theft: Reevaluating the impacts of floral larceny on plant reproductive success [J]. Plant Diversity, 2025, 47(01): 148-158.
[9]	Miao Liu, Tiancai Zhou, Quansheng Fu. Leaf nitrogen and phosphorus are more sensitive to environmental factors in dicots than in monocots, globally [J]. Plant Diversity, 2024, 46(06): 804-811.
[10]	Jun-Yi Zhang, Yue-Hong Cheng, Min Liao, Yu Feng, Sen-Long Jin, Ting-Mei He, Hai He, Bo Xu. A new infrageneric classification of Gastrochilus (Orchidaceae: Epidendroideae) based on molecular and morphological data [J]. Plant Diversity, 2024, 46(04): 435-447.
[11]	Hui Feng, Achyut Kumar Banerjee, Wuxia Guo, Yang Yuan, Fuyuan Duan, Wei Lun Ng, Xuming Zhao, Yuting Liu, Chunmei Li, Ying Liu, Linfeng Li, Yelin Huang. Origin and evolution of a new tetraploid mangrove species in an intertidal zone [J]. Plant Diversity, 2024, 46(04): 476-490.
[12]	Yumeng Ren, Lushui Zhang, Xuchen Yang, Hao Lin, Yupeng Sang, Landi Feng, Jianquan Liu, Minghui Kang. Cryptic divergences and repeated hybridizations within the endangered “living fossil” dove tree (Davidia involucrata) revealed by whole genome resequencing [J]. Plant Diversity, 2024, 46(02): 169-180.
[13]	Nian Zhou, Ke Miao, Changkun Liu, Linbo Jia, Jinjin Hu, Yongjiang Huang, Yunheng Ji. Historical biogeography and evolutionary diversification of Lilium (Liliaceae): New insights from plastome phylogenomics [J]. Plant Diversity, 2024, 46(02): 219-228.
[14]	Na Su, Richard G.J. Hodel, Xi Wang, Jun-Ru Wang, Si-Yu Xie, Chao-Xia Gui, Ling Zhang, Zhao-Yang Chang, Liang Zhao, Daniel Potter, Jun Wen. Molecular phylogeny and inflorescence evolution of Prunus (Rosaceae) based on RAD-seq and genome skimming analyses [J]. Plant Diversity, 2023, 45(04): 397-408.
[15]	Yu-Feng Gu, Jiang-Ping Shu, Yi-Jun Lu, Hui Shen, Wen Shao, Yan Zhou, Qi-Meng Sun, Jian-Bing Chen, Bao-Dong Liu, Yue-Hong Yan. Insights into cryptic speciation of quillworts in China [J]. Plant Diversity, 2023, 45(03): 284-301.