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Cryptic Self-Incompatibility and Distyly in Hedyotis Acutangula Champ

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Cryptic Self-Incompatibility and Distyly in Hedyotis Acutangula Champ See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/44648251 Cryptic self-incompatibility and distyly in Hedyotis acutangula Champ. (Rubiaceae) ARTICLE in PLANT BIOLOGY · MAY 2010 Impact Factor: 2.63 · DOI: 10.1111/j.1438-8677.2009.00242.x · Source: PubMed CITATIONS READS 16 38 3 AUTHORS, INCLUDING: Dianxiang Zhang Chinese Academy of Sciences 91 PUBLICATIONS 410 CITATIONS SEE PROFILE All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Dianxiang Zhang letting you access and read them immediately. Retrieved on: 03 December 2015 Plant Biology ISSN 1435-8603 RESEARCH PAPER Cryptic self-incompatibility and distyly in Hedyotis acutangula Champ. (Rubiaceae) X. Wu, A. Li & D. Zhang Key Laboratory of Plant Resource Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China Keywords ABSTRACT Distyly; Hedyotis acutangula; pollination; Rubiaceae; self-incompatibility; thrum Distyly, floral polymorphism frequently associated with reciprocal herkogamy, self- flowers. and intramorph incompatibility and secondary dimorphism, constitutes an impor- tant sexual system in the Rubiaceae. Here we report an unusual kind of distyly Correspondence associated with self- and ⁄ or intramorph compatibility in a perennial herb, Hedyotis D. Zhang, South China Botanical Garden, acutangula. Floral morphology, ancillary dimorphisms and compatibility of the two Chinese Academy of Sciences, Guangzhou morphs were studied. H. acutangula did not exhibit precise reciprocal herkogamy, 510650, China. but this did not affect the equality of floral morphs in the population, as usually E-mail: [email protected] found in distylous plants. Both pin and thrum pollen retained relatively high viabil- ity for 8 h. The pollen to ovule ratio was 72.5 in pin flowers and 54.4 in thrum Editor flowers. Pistils of pin flowers remained receptive for longer than those of thrum F. Roux flowers. No apparent difference in the germination rate of pin and thrum pollen grains was observed when cultured in vitro, although growth of thrum pollen tubes Received: 23 January 2009; Accepted: 22 was much faster than that of pin pollen tubes. Artificial pollination revealed that June 2009 pollen tube growth in legitimate intermorph crosses was faster than in either intra- morph crosses or self-pollination, suggesting the occurrence of cryptic self-incom- doi:10.1111/j.1438-8677.2009.00242.x patibility in this species. Cryptic self-incompatibility functioned differently in the two morphs, with pollen tube growth rates after legitimate and illegitimate pollina- tion much more highly differentiated in pin flowers than in thrum flowers. No fruit was produced in emasculated netted flowers, suggesting the absence of apomixis. Our results indicate that H. acutangula is distylous, with a cryptic self-incompati- bility breeding system. Heterostyly is believed to have developed as a mechanism INTRODUCTION to promote out-crossing (Darwin 1877). Reciprocal herkoga- Heterostyly is a genetically controlled flower polymorphism, my between morphs compels pollinators to contact the floral characterised by a reversal in the position of stigmas and organs in a particular position with the same part of their anthers in different individuals within a single population body, thus promoting intermorph pollination (Barrett 2002; (Darwin 1877; Barrett 1990). It has been estimated that het- Sanchez et al. 2008). These convergences of morphological erostylous flowers occur in at least 28 animal-pollinated flow- characters, i.e. reciprocal herkogamy and physiological mech- ering plant families, particularly in species with tubular anisms favouring intermorph pollination presented in disty- flowers (Darwin 1877; Ganders 1979; Lloyd & Webb 1992; lous species act, as an efficient mechanism to avoid self- and Barrett & Shore 2008). Heterostyly is associated with two or intramorph pollination (Lloyd & Webb 1992). However, the three morphological forms, i.e. distyly and tristyly, with vari- effectiveness of the reciprocity has been doubted due to the ations in style and filament length; there can also be differ- occurrence of different degrees of reciprocal herkogamy in ences in pollen grain morphology, and in the size of the natural populations of some species considered to be disty- stigmatic papillae and corolla (Massinga et al. 2005). The lous (Faivre & McDade 2001; Castro & Araujo 2004). Fur- main way in which heterostyly is manifest is as distyly, which thermore, fruits are not only produced by intermorph is found in more than 25 families, with new cases continu- crosses, indicating that the incompatibility mechanism in ously being reported (Eckert & Barrett 2008). In distyly, the distylous species does not always function strictly as in typical flowers of one morph have a long style and short stamens S-locus gene-controlled self-incompatibility, which mostly (pin morph), while the flowers of the other morph have a prevents self-fertilisation (Washitani et al. 1994; Castro & short style and long stamens (thrum morph). Although het- Araujo 2004; Takayama & Isogai 2005). There may thus be erostyly has received considerable attention, the origin, devel- another mechanism involved in the competitive growth of opment and transition stages leading to this polymorphism self, intramorph and outcross pollen tubes once they have still remain unsolved. reached the style. Previous studies have revealed that, once 484 Plant Biology 12 (2010) 484–494 ª 2009 German Botanical Society and The Royal Botanical Society of the Netherlands Wu, Li & Zhang Distyly in Hedyotis acutangula pollen grains have been transferred to the style in cross-polli- olla and are arranged in cymes. The petals unfold synchro- nation, pollen tube elongation is more rapid than that of nously at anthesis. Flowers open at about 07:00–08:30, and self-pollination pollen tubes, which is defined as cryptic self- last about 24 h. The anthers dehisce about 2 h before anthe- incompatibility, a phenomenon first identified 50 years ago sis. (Bateman 1956; Weller & Ornduff 1977; Alonso & Company Newly open flowers were collected and preserved in forma- 2005). Unlike species with absolute self-incompatibility, self- lin ⁄ acetic acid ⁄ alcohol (FAA). For 20 flowers in each popula- pollen tubes can arrive at the ovule and achieve successful tion, tube length, height of stigma, anther and stigma lobe fertilisation when competing cross-pollen is absent (Riveros were measured. One flower from each plant was measured. et al. 1987, 1995; Castro & Araujo 2004). However, there After corolla tube length had been recorded, flowers were have been few comprehensive demonstrations of cryptic self- dissected to allow stigma height, anther height and stigma incompatibility in distylous species. The factors that might be lobe length to be measured. Sigma and anther heights were involved in cryptic self-incompatibility, including differential measured using calipers. Corolla tube length was measured pollen viability, pollen tube growth and differences in papillae from the base of the corolla tube to the sinus. Stigma height cells on the stigma between morphs, are yet to be elucidated. was measured from the base of the corolla tube to the tip of Rubiaceae is the fourth largest angiosperm family and the stigma lobe. Anther height was measured from the base contains the largest number of distylous genera (Ganders of the corolla tube to the tip of the anther, since the fila- 1979). Based on previous classification systems and phyloge- ments are thin and attached to the sides of corolla tubes. netic analyses of the Rubiaceae, the genus Hedyotis L. is Stigma lobe length was measured from the apex of the style included in the tribe Hedyotideae (Spermacoceae) and sub- to the tip of the stigma lobes. The pollen–ovule ratio (P ⁄ O) family Rubioideae (Robbrecht 1988; Bremer et al. 1995, was estimated using the method described by Dafni (1992) 1999; Bremer & Manen 2000; Robbrecht & Manen 2006). In from 20 pin and 20 thrum plants in each population. The a recent phylogenetic analysis, the monophyletic status of pollen grains in one anther from each bud were carefully dis- tribe Spermacoceae has been strongly supported, but the sected out, and transferred to calibrated tubes containing genus Hedyotis has been suggested only to include the Asian 0.5 ml distilled water. The suspension was stirred and 10–15 species in a clade that is sister to the clade that includes the separate samples of 1 ll each were transferred to a micro- genera Agathisanthemum, Lelya and three Oldenlandia species scope slide. Finally, the pollen grains were counted under the (one from North America, and two from Africa) (Ka˚rehed microscope. Ovaries were carefully dissected out of each et al. 2008). The genus Hedyotis has a broad spectrum of flower and placed in a drop of water on a microscope slide, breeding systems, including distyly, dioecy and herkogamy and all ovules counted. Nectar production was also compared (Robbrecht 1988; Wagner & Lorence 1998; Ko 1999). Previ- for each bagged flower from 10 pin and 10 thrum plants ous studies have demonstrated that pollen dimorphism with in each population. Nectar was collected with a 0.5-ll respect to size, shape and exine characteristics, occurs in microcapillary 4 h after anthesis. Sugar content was measured some distylous species of the Rubiaceae (Naiki & Nagamasu as sucrose equivalents using a portable refractometer (Brix 2003; Castro et al. 2004).
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