黑果枸杞两种花型的花部综合征与传粉特性
收稿日期: 2021-12-09
录用日期: 2022-05-07
网络出版日期: 2022-10-11
基金资助
国家自然科学基金(31860121);“天山雪松计划”青年拔尖人才后备人选培养项目和新疆维吾尔自治区高层次人才培养计划项目(QN2016BS0597)
Flower syndrome and pollination characteristics of two flower morphs in Lycium ruthenicum (Solanaceae)
Received date: 2021-12-09
Accepted date: 2022-05-07
Online published: 2022-10-11
Supported by
National Natural Science Foundation of China(31860121);“Tianshan Xuesong” Young Top Talent Reserve Project and the High-level Personnel Training Program of the Xinjiang Uygur Autonomous Region(QN2016BS0597)
黑果枸杞(Lycium ruthenicum)是中国西北地区极端环境中分布的国家二级保护植物, 该物种在新疆南部的自然种群中出现了同型花柱类型(同位花)和柱头探出式雌雄异位类型(异位花)个体, 并且遭遇沙尘暴频繁的种群中异位花个体出现频率减少。该研究对喀什市自然种群中黑果枸杞两种不同花型植株的花部综合征和传粉特性进行比较研究, 以期探讨该物种不同花型植株在南疆早春极端环境中的花部特征的可塑性及其适应性机制。结果表明: 同位花雌雄蕊高度间无显著差异, 而异位花雌蕊高度显著高于雄蕊; 同位花花冠直径、花冠筒长、胚珠数均高于异位花, 而异位花雌雄蕊空间距离、花粉数及花粉胚珠比均比同位花高。黑果枸杞同位花个体比例(68%)高于异位花个体(32%), 种群水平及个体水平同位花花期((117.00 ± 2.25) d, (101.65 ± 1.98) d)比异位花((26.00 ± 1.00) d, (18.75 ± 1.00) d)长, 而单花水平上异位花单花寿命((4.50 ± 0.14) d)比同位花((3.13 ± 0.11) d)长。两种类型花在花早期(紫色)分泌的花蜜量均高于花后期(白色)。在紫色花阶段(花开放早期), 同位花上的主要传粉者意大利蜜蜂、熊蜂和食蚜蝇的访花频率和停留时间均高于异位花; 而白色花阶段(花开放后期)意大利蜜蜂、熊蜂在异位花上的访花频率比同位花高。在不同花色阶段, 同位花柱头花粉落置数、花粉移出率、花粉传递效率均比异位花高, 并且同位花自然坐果率及结籽率均比异位花高。在新疆南部的沙尘暴极端环境下, 同位花通过较高的自交亲和性保障繁殖, 而异交为主的异位花提高了异交率。异位花与同位花在花部综合征和花报酬上的差异, 是影响其繁殖成功的主要因素。
哈里布努尔, 古丽扎尔·阿不都克力木, 热依拉穆·麦麦提吐尔逊, 艾沙江·阿不都沙拉木 . 黑果枸杞两种花型的花部综合征与传粉特性[J]. 植物生态学报, 2022 , 46(9) : 1050 -1063 . DOI: 10.17521/cjpe.2021.0463
Aims Flower syndrome and pollination characteristics are the basis and main driving forces of the evolutionary success of flowering plants. Lycium ruthenicum is a national second-class protected plant distributed in northwest China, with two flower morphs, i.e. homostylous flower (style length is similar to stamen length) and flower with approach herkogamy (style length is longer than stamen length). However, little is known about the flower syndrome and pollination characteristics of the different flower types of L. ruthenicum.
Methods In this study, we compared the flowering phenology, flower characteristics, flower reward, and pollination characteristics of two different flower morphs of L. ruthenicum.
Important findings In Kashi natural populations, there is no significant difference in the height of sexual organs of homostylous flower, but it is significant in the herkogamous flowers. The corolla diameter, corolla tube length, number of ovules of homostylous flowers are higher than that of herkogamous flowers. The stamen-stigma distance, number of pollen and pollen/ovule (P/O) of herkogamous flowers are higher than that of homostylous flower. The proportion of homostylous individuals (68%) is higher than that of herkogamous (32%). Population and individual level flowering times were significantly different between the flower morphs and were longer for homostylous flower individuals ((117.00 ± 2.25) d, (101.65 ± 1.98) d) than that of herkogamous flower individuals ((26.00 ± 1.00) d, (18.75 ± 1.00) d), but the longevity of herkogamy flowers ((4.50 ± 0.14) d) are longer than that of homostylous flowers ((3.13 ± 0.11) d). At early flower stage (purple phase) the nectar volume of two morphs is significantly higher than late stage (white phase). In the purple phase the main pollinators were Bombussp., Apis mellifera and Syrphidae, and the visiting frequency and duration of stay on the homostylous flowers are higher than that of herkogamy flowers. In the white phase, the main pollinators on the herkogamous flower have higher visiting frequency than that of homostylous flower. At the different phases the number of pollen deposited on the stigma, pollen removal rate, pollination efficiency of homostylous flowers are higher than that of herkogamous flowers. The fruit and seed set of homostylous flowers are higher than that of herkogamous flowers. Under the extreme environment of sandstorms in southern Xinjiang, homostylous flowers can secure reproduction through high self-compatibility, and herkogamous flowers will increase outcrossing rate in the population. These differences in flower traits and pollination adaptations may be the main factor affecting the reproductive success of L. ruthenicum.
| [1] | Abdusalam A, Abdukirim G (2018). Pollination characteristics of two sympatrically distributed Tamarix species in south Xinjiang, China. Plant Science Journal, 36, 162-169. |
| [1] | [艾沙江·阿不都沙拉木, 古丽扎尔·阿不都克力木 (2018). 同域分布柽柳属两种植物的传粉生物学研究. 植物科学学报, 36, 162-169.] |
| [2] | Abdusalam A, Maimaitituerxun R, Hashan H, Abdukirim G (2021). Pollination adaptations of group-by-group stamen movement in a meadow plant with temporal flower closure. Plant Diversity, 43, 308-316. |
| [3] | Abdusalam A, Tan DY (2014). Contribution of temporal flower closure to reproductive success of the spring-flowering Tulipa iliensis. Journal of Systematics and Evolution, 52, 186-194. |
| [4] | Arroyo MTK, Armesto JJ, Primack RB (1985). Community studies in pollination ecology in the high temperate Andes of central Chile. II. Effect of temperature on visitation rates and pollination possibilities. Plant Systematics and Evolution, 149, 187-203. |
| [5] | 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 Phytologist, 200, 1260-1268. |
| [6] | Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004). Pollen limitation of plant reproduction ecological and evolutionary causes and consequences. Ecology, 85, 2408-2421. |
| [7] | Ashman TL, Schoen DJ (1994). How long should flowers live? Nature, 371, 788-791. |
| [8] | Barrett SCH (1998). The evolution of mating strategies in flowering plants. Trends in Plant Science, 3, 335-341. |
| [9] | Barrett SCH (2003). Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 358, 991-1004. |
| [10] | Barrett SCH (2010). Understanding plant reproductive diversity. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 365, 99-109. |
| [11] | Barrett SCH, Harder LD (1996). Ecology and evolution of plant mating. Trends in Ecology & Evolution, 11, 73-79. |
| [12] | Barrett SCH, Jesson LK, Baker AM (2000). The evolution and function of stylar polymorphisms in flowering plants. Annals of Botany, 85, 253-265. |
| [13] | Bhatnagar S, Meena D, Singh S (2019). Effect of climate change on plants and their pollinators: a review. International Journal of Biotech Trends and Technology, 9, 34-39. |
| [14] | Bingham RA, Orthner AR (1998). Efficient pollination of alpine plants. Nature, 391, 238-239. |
| [15] | Bonamour S, Chevin LM, Charmantier A, Teplitsky C (2019). Phenotypic plasticity in response to climate change: the importance of cue variation. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 374, 20180178. DOI: 10.1098/rstb.2018.0178. |
| [16] | Bosch J, Blas M (1994). Foraging behaviour and pollinating efficiency of Osmia cornuta and Apis mellifera on almond (Hymenoptera: Megachilidae, Apidae). Applied Entomology and Zoology, 29, 1-9. |
| [17] | Brummell DA, Harpster MH, Dunsmuir P (1999). Differential expression of expansin gene family members during growth and ripening of tomato fruit. Plant Molecular Biology, 39, 161-169. |
| [18] | Campbell DR, Waser NM, Price MV (1996). Mechanisms of hummingbird-mediated selection for flower width in Ipomopsis aggregata. Ecology, 77, 1463-1472. |
| [19] | Charlesworth D, Charlesworth B (1979). A model for the evolution of distyly. The American Naturalist, 114, 467-498. |
| [20] | Cheptou PO (2012). Review: part of a special issue on plant mating systems, Clarifying Baker’s Law. Annals of Botany, 109, 633-641. |
| [21] | Clark MJ, Husband BC (2007). Plasticity and timing of flower closure in response to pollination in Chamerion angustifolium (Onagraceae). International Journal of Plant Science, 168, 619-625. |
| [22] | Dafni A, Kevan PG, Husband BC (2005). Practical Pollination Biology. Enviroquest, Ontario, Canada. 130-141. |
| [23] | Dai GL, Qin K, Cao YL, Jiao EN, Zhang B (2013). Characteristics of flower dynamic and breeding system of Lycium ruthenicum. Guihaia, 33, 126-132. |
| [23] | [戴国礼, 秦垦, 曹有龙, 焦恩宁, 张波 (2013). 黑果枸杞的花部结构及繁育系统特征. 广西植物, 33, 126-132.] |
| [24] | Darwin C (1872). The Different Forms of Flowers on Plants of the Same Species. D. Appleton and Co, New York. |
| [25] | Duan YW, He YP, Zhang TF, Liu JQ (2007). Delayed selfing in an alpine species Gentianopsis barbata. Journal of Plant Ecology, 31, 110-117. |
| [25] | [段元文, 何亚平, 张挺锋, 刘建全 (2007). 高山植物扁蕾的延迟自交机制. 植物生态学报, 31, 110-117.] |
| [26] | Elliott SE, Irwin RE (2009). Effects of flowering plant density on pollinator visitation, pollen receipt, and seed production in Delphinium barbeyi (Ranunculaceae). American Journal of Botany, 96, 912-919. |
| [27] | Etcheverry AV, Alemán MM, Fleming TF (2008). Flower morphology, pollination biology and mating system of the complex flower of Vigna caracalla (Fabaceae: papilionoideae). Annals of Botany, 102, 305-316. |
| [28] | Gao JY, Yang ZH, Li QJ (2009). Effects of flower longevity on male and female fitness in Hedychium villosum var. villosum. Chinese Journal of Plant Ecology, 33, 89-96. |
| [28] | [高江云, 杨自辉, 李庆军 (2009). 毛姜花原变种花寿命对两性适合度的影响. 植物生态学报, 33, 89-96.] |
| [29] | Gong YB, Huang SQ (2014). Interspecific variation in pollen- ovule ratio is negatively correlated with pollen transfer efficiency in a natural community. Plant Biology, 16, 843-847. |
| [30] | Harder LD, Johnson SD (2009). Darwin’s beautiful contrivances: evolutionary and functional evidence for flower adaptation. New Phytologist, 183, 530-545. |
| [31] | He YP, Duan YW, Liu JQ, Smith WK (2005). Flower closure in response to temperature and pollination in Gentiana straminea Maxim. (Gentianaceae), an alpine perennial in the Qinghai-Tibetan Plateau. Plant Systematics and Evolution, 256, 17-33. |
| [32] | Hou QZ, Duan YW, Si QW, Yang HL (2009). Pollination ecology of Gentiana lawrencei var. farreri, a late-flowering Qinghai-Tibet Plateau species. Chinese Journal of Plant Ecology, 33, 1156-1164. |
| [32] | [侯勤正, 段元文, 司庆文, 杨慧玲 (2009). 青藏高原晚期开花植物线叶龙胆的传粉生态学. 植物生态学报, 33, 1156-1164.] |
| [33] | Huang SQ, Guo YH (2000). Advances in pollination biology. Chinese Science Bulletin, 45, 225-237. |
| [33] | [黄双全, 郭友好(2000). 传粉生物学的研究进展. 科学通报, 45, 225-237.] |
| [34] | Hudabaierdi M, Pan XL (2004). Flora Xinjianggensis: Tomus 4. Xinjiang Science & Technology Publishing House, ürümqi. 353-354. |
| [34] | [米吉提·胡达拜尔地, 潘晓玲 (2004). 新疆植物志(第四卷). 新疆科学技术出版社, 乌鲁木齐,354-355.] |
| [35] | Ida TY, Kudo G (2010). Modification of bumblebee behavior by flower color change and implications for pollen transfer in Weigela middendorffiana. Evolutionary Ecology, 24, 671-684. |
| [36] | Ishii HS, Sakai S (2002). Temporal variation in flower display size and individual flower sex allocation in racemes of Narthecium asiaticum (Liliaceae). American Journal of Botany, 89, 441-446. |
| [37] | Ivey CT, Carr DE (2011). Tests for the joint evolution of mating system and drought escape in Mimulus. Annals of Botany, 109, 583-598. |
| [38] | Li QJ, Xu ZF, Kress WJ, Xia YM, Zhang L, Deng XB, Gao JY, Bai ZL (2001). Flexible style that encourages outcrossing. Nature, 410, 432. DOI: 10.1038/35068635. |
| [39] | Navarro L, Ayensa G, Guitián P (2007). Adaptation of flower traits and mating system to pollinator unpredictibility: the case of Disterigma stereophyllum (Ericaceae) in southwestern Colombia. Plant Systematics and Evolution, 266, 165-174. |
| [40] | Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F,van Kleunen M (2010). Plant phenotypic plasticity in a changing climate. Trends in Plant Science, 15, 684-692. |
| [41] | Nishihiro J, Washitani I, Thomson JD, Thomson BA (2000). Patterns and consequences of stigma height variation in a natural population of a distylous plant Primula sieboldii. Functional Ecology, 14, 502-512. |
| [42] | Nuttman CV, Semida FM, Zalat S, Willmer PG (2006). Visual cues and foraging choices: bee visits to flower colour phases in Alkanna orientalis (Boraginaceae). Biological Journal of the Linnean Society, 87, 427-435. |
| [43] | Oliveira LC, Matias R, Furtado MT, Romero R, Brito VLG (2022). What explains the variation in length of stamens and styles in a pollen flower? A study exemplified by Macairea radula (Melastomataceae). Plant Systematics and Evolution, 308, 1-13. |
| [44] | Ollerton J, Winfree R, Tarrant S (2011). How many flowering plants are pollinated by animals? Oikos, 120, 321-326. |
| [45] | Pacheco DA, Dudley LS, Cabezas J, Cavieres LA, Arroyo MTK (2016). Plastic responses contribute to explaining altitudinal and temporal variation in potential flower longevity in high Andean Rhodolirion montanum. PLOS ONE, 11, e0166350. DOI: 10.1371/journal.pone.0166350. |
| [46] | Primack RB (1985). Longevity of individual flowers. Annual Review of Ecology and Systematics, 16, 15-37. |
| [47] | Ruan CJ, Qin P, Yin ZF (2006). Advancements in reproductive assurance and delayed selfing. Acta Ecologica Sinica, 26, 195-204. |
| [47] | [阮成江, 钦佩, 尹增芳 (2006). 繁殖保障和延迟自交的研究进展. 生态学报, 26, 195-204.] |
| [48] | Shi YH, Ren ZX, Zhao YH, Wang H (2021). Effect of climate change on the distribution and phenology of plants, insect pollinators, and their interactions. Biodiversity Science, 29, 495-506. |
| [48] | [施雨含, 任宗昕, 赵延会, 王红 (2021). 气候变化对植物-传粉昆虫的分布区和物候及其互作关系的影响. 生物多样性, 29, 495-506.] |
| [49] | Shivanna KR, Tandon R, Koul M (2020). “Global Pollinator Crisis” and its impact on crop productivity and sustenance of plant diversity//Tandon R, Shivanna KR, Koul M. Springer, |
| [50] | Spigler RB, Kalisz S (2013). Phenotypic plasticity in mating- system traits in the annual Collinsia verna. Botany, 91, 597-604. |
| [51] | Sun S, Cao GX, Luo YJ, Li QJ (2010). Maintenance and functional gender specialization of flexistyly. Chinese Journal of Plant Ecology, 34, 827-838. |
| [51] | [孙杉, 操国兴, 罗燕江, 李庆军 (2010). 花柱卷曲性的维持及功能性别特化. 植物生态学报, 34, 827-838.] |
| [52] | Sun SG, Guo YH, Gituru RW, Huang SQ (2005). Corolla wilting facilitates delayed autonomous self-pollination in Pedicularis dunniana (Orobanchaceae). Plant Systematics and Evolution, 251, 229-237. |
| [53] | Tang XX, Huang SQ (2012). Research progress on diversity and variation in flower color. Plant Diversity and Resources, 34, 239-247. |
| [53] | [汤晓辛, 黄双全 (2012). 花色多样性与变异的研究进展. 植物分类与资源学报, 34, 239-247.] |
| [54] | Torres-Díaz C, Gómez-González S, Stotz GC, Torres-Morales P, Paredes B, Pérez-Millaqueo M, Gianoli E (2011). Extremely long-lived stigmas allow extended cross- pollination opportunities in a high Andean plant. PLOS ONE, 6, e19497. DOI: 10.1371/journal.pone.0019497. |
| [55] | Wang XY, Zhu XX, Yang J, Liu YJ, Tang XX (2019). Variation in style length and the effect on reproductive success in Chinese plums (Armeniaca mume). Biodiversity Science, 27, 159-167. |
| [55] | [王晓月, 朱鑫鑫, 杨娟, 刘云静, 汤晓辛 (2019). 梅花个体内花柱长度的变异及其对繁殖成功的影响. 生物多样性, 27, 159-167.] |
| [56] | Webb CJ, Lloyd DG (1986). The avoidance of interference between the presentation of pollen and stigmas in angiosperms II. Herkogamy. New Zealand Journal of Botany, 24, 163-178. |
| [57] | Wiemer AP, Sérsic AN, Marino S, Sim?es AO, Cocucci AA (2011). Functional morphology and wasp pollination of two south American asclepiads (Asclepiadoideae- Apocynaceae). Annals of Botany, 109, 77-93. |
| [58] | Wu Y, Liu YR, Peng H, Yang Y, Liu GL, Cao GX, Zhang Q (2015). Pollination ecology of alpine herb Meconopsis integrifolia at different altitudes. Chinese Journal of Plant Ecology, 39, 1-13. |
| [58] | [吴云, 刘玉蓉, 彭瀚, 杨勇, 刘光立, 操国兴, 张强 (2015). 高山植物全缘叶绿绒蒿在不同海拔地区的传粉生态学研究. 植物生态学报, 39, 1-13.] |
| [59] | Xiang WQ, Ren MX (2019). Adaptive significance of yellow flowered Bombax ceiba (Malvaceae). Biodiversity Science, 27, 373-379. |
| [59] | [向文倩, 任明迅 (2019). 木棉黄花个体的适应意义. 生物多样性, 27, 373-379.] |
| [60] | Zhang DY (2004). Plant Life-History Evolution and Reproductive Ecology. Science Press, Beijing. 96-180. |
| [60] | [张大勇 (2004). 植物生活史进化与繁殖生态学. 科学出版社, 北京. 96-180.] |
| [61] | Zhang DY, Jiang XH (2001). Mating system evolution, resource allocation, and genetic diversity in plants. Acta Phytoecologica Sinica, 25, 130-143. |
| [61] | [张大勇, 姜新华 (2001). 植物交配系统的进化、资源分配对策与遗传多样性. 植物生态学报, 25, 130-143.] |
| [62] | Zhang L, Li QJ (2002). Flexistyly and its evolutionary ecological significance. Acta Phytoecologica Sinica, 26, 385-390. |
| [62] | [张玲, 李庆军 (2002). 花柱卷曲性异交机制及其进化生态学意义. 植物生态学报, 26, 385-390.] |
| [63] | Zhang ZQ, Li QJ (2009). Review of evolutionary ecology of flower longevity. Chinese Journal of Plant Ecology, 33, 598-606. |
| [63] | [张志强, 李庆军 (2009). 花寿命的进化生态学意义. 植物生态学报, 33, 598-606.] |
| [64] | Zych M, Junker RR, Nepi M, Stpiczyńska M, Stolarska B, Roguz K (2018). Spatiotemporal variation in the pollination systems of a supergeneralist plant: Is Angelica sylvestris (Apiaceae) locally adapted to its most effective pollinators? Annals of Botany, 123, 415-428. |
/
| 〈 |
|
〉 |
