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Induced Cleistogamy: a Strategy for Reproductive Assurance in Murdannia Nudiflora (Commelinaceae)

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Induced Cleistogamy: a Strategy for Reproductive Assurance in Murdannia Nudiflora (Commelinaceae) Botany Induced cleistogamy: A strategy for reproductive assurance in Murdannia nudiflora (Commelinaceae) Journal: Botany Manuscript ID cjb-2019-0007.R3 Manuscript Type: Article Date Submitted by the 25-Jun-2019 Author: Complete List of Authors: V, VEENA; University of Calicut, BOTANY Nampy, Santhosh; University of Calicut anthesis, breeding systems, chasmogamous, entomophilous, Keyword: spontaneousDraft autogamy Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/botany-pubs Page 1 of 34 Botany Induced cleistogamy: A strategy for reproductive assurance in Murdannia nudiflora (Commelinaceae) Veena V. & *Santhosh Nampy Department of Botany, University of Calicut, Malappuram District, Kerala, India- 673635 *[email protected], [email protected] *Corresponding Author Draft 1 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 2 of 34 Abstract Murdannia nudiflora is a day flower that is dependent on entomophilous pollination. Despite the lack of pollinator attractants, and its short flower longevity, M. nudiflora shows high fecundity rates, which lead to their quick dispersal. In addition to monitoring vegetative reproductive methods and the effect of select environmental parameters (atmospheric temperature, relative humidity, and precipitation rates), we evaluated mating systems in this species via artificial crosses. This species has evolved to undergo autogamy to ensure reproductive success for when pollinators are insufficient; cleistogamous flowers are produced for optimal pollinator activity when environmental conditions are unfavorable. The number of cleistogamous flowers produced was foundDraft to be positively correlated with humidity and precipitation rates, and negatively correlated with temperature. In addition, it was found that high humidity and precipitation always hinder insect pollinators. Therefore, the combination of vegetative reproduction, entomophily, and cleistogamous self-pollination helps this weedy species to propagate to its maximum efficiency. M. nudiflora employs pre-anthesis cleistogamy as a mating strategy for reproductive assurance while retaining mechanisms that promote out-crossing. Key words: anthesis; breeding systems; chasmogamous; entomophilous; pollen viability; spontaneous autogamy. 2 https://mc06.manuscriptcentral.com/botany-pubs Page 3 of 34 Botany Introduction Murdannia Royle is a genus within the dayflower family Commelinaceae, which includes 56 species worldwide. The genus is primarily Asiatic, with species inhabiting diverse habitats. Murdannia nudiflora (L.) Brenan, one of the most widespread species of this genus (Ancy and Nampy 2015), was reported to be invasive (Faden 1982, 2000; GCW 2007) in most parts of the United States, Central and South Americas, and western Australia (Keighery 1982; Waterhouse 1993; Faden 2000). It is classified as one of the world's worst weeds, infesting no less than 16 crops in 23 countries (Holm et al. 1977; Moody 1989). Draft Murdannia nudiflora are usually erect to decumbent herbs with rarely branched tufted shoots and roots at the nodes. Its flowers are bisexual (rarely unisexual) and are compactly arranged on the inflorescence axis (Ancy and Nampy 2015). Despite the short blooming period of its flowers, M. nudiflora shows high reproductive success and propagation from one growing season to the next. Like most members of the Commelinaceae family, M. nudiflora uses entomophily as its chief mode of pollination. Generally, short duration of flower opening and a lack of nutritional rewards other than pollen (Faden 1992) for pollinators limit population increase by sexual methods in entomophilous species. Arguably, this species may be relying on vegetative propagation to ensure continuous population increase. Though their ability to root readily at nodes and propagate clonally through stems attests to their potential for vegetative propagation, these ‘propagules’ are unable to survive the harsh summer and perennate to the next season. Contrary to expectations, the Invasive Species Compendium (Centre for Agriculture and Biosciences International, https://www.cabi.org/isc/datasheet/35180) reported that M. nudiflora produces 500-2200 seeds per plant, which is a relatively high number for a plant with a short flowering time, lacks nectar, and 3 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 4 of 34 is dependent on insect pollinators. In this study, we aimed to unravel the strategies for reproductive assurance in M. nudiflora across seasons. Materials and methods Study area Natural populations of M. nudiflora growing in the Calicut University Botanical Garden (CUBG, 11⁰7.9850'N 75⁰53.3710'E), Malappuram District, Kerala, and Vellimadukunnu (VK, 11⁰18.1070'N 75⁰48.9250E), Kozhikode District, Kerala, separated by a distance of 30 km, were studied over the course of two years (2016-2017). The first populationDraft was comprised of 73 plants spread over a 3 × 2 m plot, and the second population contained 30 plants spread over a 1 × 1 m plot. Data on humidity, temperature, and precipitation were recorded and pooled. Floral morphology and phenology Inflorescence of M. nudiflora is terminal and axillary, consisting of single or sometimes paired pedunculate cincinni. The flowers are usually bisexual and are very rarely male. They are compactly arranged in the cincinnus, and are trimerous with free, ovate-elliptic, pale green, glabrous sepals, and free, obovate, and lilac to lavender colored petals. There are two antesepalous stamens, which are dorsifixed with dense hairs at the basal half of the filament. Anther lobes are deep bluish purple with purplish-white connectives, and dehisce longitudinally to release ellipsoid, creamy-yellowish white pollen. There are four staminodes, of which three are antepetalous and one is antesepalous. They are either glabrous or possess a few hairs at the base with trilobed, white antherodes; the antherode of the antisepalous staminode is reduced to a knob. The ovary is greenish and glabrous, while the style is white, with papillate stigma. Capsules are ellipsoid-triangular, with two uniseriate seeds in each locule (Fig. 1. A-F). 4 https://mc06.manuscriptcentral.com/botany-pubs Page 5 of 34 Botany We randomly chose 10 chasmogamous and 10 cleistogamous flowers from each of the populations. Floral traits, including lengths of sepals, petals, stamens, and staminodes, were compared using a Zeiss Stemi 508 stereomicroscope. Floral phenoevents were recorded for one hour between anthesis and flower closure. A total of 35 inflorescences (20 at the first site and 15 at the second) were observed on 20 random days in each season. A total of 234 flowers were studied. Pollen production Pollen production for 10 flowers from the CalicutDraft University Botanical Garden (CUBG) was studied with a hemocytometer (Shore and Barrett 1984; Barrett 1985; Dudash 1991); mean value was estimated. Pollen dispersal To study pollen dispersal, pollen traps were set by fixing microscope cover-slides on wooden sticks to the ground at the level of the inflorescence, facing the direct of the prevailing wind (Mulugata et al. 1994). Ten traps were set each day for 25 days every season, before anthesis. Following flower closure, traps were removed and compared with a known sample under the microscope. Observations were made on floral visitors for 15 days each season, from anthesis to flower closure. The number of floral visitors, visiting time, foraging nature, foraging hour, time spent in each flower, stigma touch by insects, and frequency of their visits were recorded; the presence of pollen on pollinators was confirmed. Insects were identified with assistance from the Division of Entomology, Department of Zoology, University of Calicut. Pollen viability 5 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 6 of 34 Pollen viability tests were carried out in flowers taken from the CUBG. To determine pollen viability, the 1,2,3-triphenyl tetrazolium chloride (TTC) method (Shivanna and Rangaswamy 1992) was used. Tests were carried out at one-hour intervals on freshly collected pollen for two days each season. Pistil receptivity The stigma receptivity period was tested (at CUBG) at one-hour intervals with the α-naphthyl acetate test (Pearse 1985); results were confirmed via in vivo germination tests. The pollinated stigmas were fixed at various periods, and only those that supported pollen germination were considered to be receptive. Breeding system and fruit set Draft Twenty-five randomly selected flowers from each of the two populations were subjected to seven pollination treatments, as outlined below (Kaul and Koul 2008): 1. Flowers were tagged before anthesis and left for natural pollination to provide estimates of fruit set under natural conditions. 2. Flowers were emasculated before anthesis and were left for natural pollination. 3. Flowers were left for natural pollination with anthers and staminodes removed; filaments were retained. 4. Manual cross-pollination of emasculated flowers followed by bagging to evaluate cross- compatibility. 5. Manual self-pollination of emasculated flowers followed by bagging to test for self-compatibility. 6. Bagging flower buds to evaluate autonomous selfing. 7. Cleistogamous flowers were tagged to estimate fruit set. 6 https://mc06.manuscriptcentral.com/botany-pubs Page 7 of 34 Botany For manual self-pollination, pollen grains were collected either from the same flower or from another flower of the same plant. For
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