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Seed Dormancy in Campanulaceae: Morphological and Morphophysiological Dormancy in Six Species of Hawaiian Lobelioids

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Seed Dormancy in Campanulaceae: Morphological and Morphophysiological Dormancy in Six Species of Hawaiian Lobelioids Botany Seed dormancy in Campanulaceae: morphological and morphophysiological dormancy in six species of Hawaiian lobelioids Journal: Botany Manuscript ID cjb-2020-0009.R1 Manuscript Type: Article Date Submitted by the 03-Mar-2020 Author: Complete List of Authors: Baskin, Carol; University of Kentucky, Biology Baskin, Jerry; University of Kentucky, Biology Yoshinaga, Alvin; Center for Conservation Research and Training Wolkis, Dustin;Draft National Tropical Botanical Garden, Department of Science & Conservation embryo growth, endemic species, morphological dormancy, Keyword: morphophysiological dormancy, seed dormancy Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/botany-pubs Page 1 of 19 Botany 1 Seed dormancy in Campanulaceae: morphological and morphophysiological dormancy in 2 six species of Hawaiian lobelioids 3 4 Carol C. Baskin, Jerry M. Baskin, Alvin Yoshinaga and Dustin Wolkis 5 6 Carol C. Baskin [email protected] 7 Department of Biology, University of Kentucky, Lexington, KY 40506 USA 8 Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546 USA 9 10 Jerry M. Baskin [email protected] 11 Department of Biology, University of Kentucky, Lexington, KY 40506 USA 12 13 Alvin Yoshinaga [email protected] 14 Center for Conservation Research and Training, 3050 Maile Way, Gilmore No. 409, Honolulu, HI 15 96822 USA 16 Dustin Wolkis [email protected] 17 Department of Science and Conservation, National Tropical Botanical Garden, 3530 Papalina 18 Road, Kalāheo, HI 96741 19 20 Running title: Germination of Hawaiian lobelioids 21 22 Author for correspondence Carol C. Baskin: [email protected] 23 1 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 2 of 19 24 Abstract 25 We determined the requirements for dormancy break/germination and kind of dormancy in 26 seeds of the Hawaiian lobelioids Cyanea kunthiana, Delissea rhytidoperma, Lobelia grayana, L. 27 hypoleuca, Trematolobelia grandifolia and T. singularis. Fresh seeds were incubated in 28 light/dark at 15/6, 20/10 and 25/15°C and germination monitored at 2-week intervals for 14 29 weeks. For each species, the mean embryo length (E) : seed (S) length ratio was determined for 30 freshly-matured seeds and for seeds at the time the seed coat split but before radicle emergence 31 (germination). The embryo in seeds of all six species incubated at 25/15°C grew inside the seed 32 prior to germination (42-148% increase in E:S ratio, depending on species). Seeds of L. grayana 33 and L. hypoleuca have morphological dormancy; they germinated to 82-98% at the three 34 temperature regimes in 4 weeks. Seeds ofDraft the other species have nondeep simple 35 morphophysiological dormancy and require >4 weeks for maximum germination to occur. Our 36 results add to the growing body of knowledge about the kind (class) of seed dormancy in 37 Campanulaceae, which suggests that seeds of members of this family have either MD or MPD 38 and embryos grow at warm (≥ 15°C) temperatures. 39 40 Keywords: embryo growth, endemic species, morphological dormancy, morphophysiological 41 dormancy, seed dormancy 42 2 https://mc06.manuscriptcentral.com/botany-pubs Page 3 of 19 Botany 43 Introduction 44 The eudicot family Campanulaceae (APG 2016) consist of herbaceous annuals, biennials and 45 perennials and includes pachycaul rosette plants, subshrubs, shrubs, treelets, trees to 15 m tall 46 (Lammers 2007) and some aquatics (Mabberley 2008). The family is divided into five 47 subfamilies (Campanuloideae, Lobelioideae, Nemacladoideae, Cyphioideae and 48 Cyphocarpoideae) and contains 84 genera and nearly 2400 species (Antonelli 2007; Lammers 49 2007; Crowl et al. 2014). According to Lammers (2007), 25, 25, 18, 11, 11, 6 and 4 % of the 50 species of Campanulaceae occur in Africa, South America, Asia, Europe, North America, 51 Polynesia and Australia, respectively. South Africa has 18 genera and nearly 400 species, and it 52 is the only region with a large number ofDraft both Campanulioideae and Lobelioideae; the 53 Cyphioideae with 64 species is restricted to Africa. Other centers of distribution predominantly 54 have only Campanuloideae or Lobelioideae. For example, in the Hawaiian Islands, there are six 55 genera and 126 species of Lobelioideae (Givnish et al. 2009, 2013), representing the largest 56 family of Hawaiian angiosperms (Wagner 1999), i.e. the largest plant species radiation in Hawaii 57 (Givnish et al. 2009). All the native Campanulaceae in Hawaii belong to the Lobelioideae 58 (Wagner 1999). 59 The Afrotropics are the inferred ancestral place of origin of the Campanulaceae, 60 including Lobelioideae (Crowl et al. 2016). Antonelli (2009) found that the giant lobelias of 61 eastern Africa, South America, Hawaiian Islands, French Polynesia and southeast Asia form a 62 monophyletic group and suggested that they are derived from a woody ancestor that grew in 63 Africa. Using molecular phylogeny data, Givnish et al. (2009) showed that the Lobelioideae in 64 Hawaii are from one immigration event. The lobelioids have diversified in Hawaii and can be 65 found in a wide range of habitats and exhibit diversity in growth form, pollination biology 3 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 4 of 19 66 (Givnish et al. 2009) and seed coat morphology (Buss et al. 2001), but except for Clermontia 67 fauriei, C. hawaiiensis, C. kakeana, C. pyrularia, Cyanea angustifolia and Trematolobelia 68 macrostachys (Baskin et al. 2005), we have limited knowledge about seeds of the Hawaiian 69 lobelioids. 70 For the Campanulaceae, a relatively short linear embryo and copious endosperm occur in 71 the seeds of Campanula, Clermontia, Cyanea, Delissea, Lobelia,, Trematolobelia, Triodanis and 72 Wahlenbergia (Baskin and Baskin unpublished embryo data base). Seeds of L. dentata and 73 perhaps other species in the Australian endemic section Holopogon of Lobelia (sensu Lammers, 74 2011) have an undifferentiated embryo (Fraser 1931; Warcup 1988). In the seeds of temperate- 75 zone Campanula americana, Lobelia appendiculataDraft and L. spicata (Baskin and Baskin 2005) 76 and the Hawaiian lobelioid shrubs Clermontia fauriei, C. hawaiiensis, C. kakeana, C. pyrularia, 77 Cyanea angustifolia and Trematolobelia macrostachys (Baskin et al. 2005), the embryo grows 78 inside the seed prior to germination (radicle emergence). If embryo growth and germination in 79 freshly-matured seeds occur over a wide range of temperatures during incubation for about 4 80 weeks, seeds have morphological dormancy (MD), i.e. no physiological dormancy (PD) and 81 germination is delayed until the embryo grows to its full length (Nikolaeva 1977; Baskin and 82 Baskin 2014). On the other hand, freshly matured seeds have morphophysiological dormancy 83 (MPD) if dormancy-breaking treatments are required to break the PD component of dormancy 84 and embryo growth and germination take longer than 4 weeks. If seeds with MPD germinate at 85 some temperatures in about 4 weeks but over a wider temperature range after 4 weeks, MPD is 86 conditional, i.e. conditional MPD. Seeds of C. americana have MD, while those of C. fauriei, C. 87 hawaiiensis, C. kakeana, C. pyrularia, C. angustifolia, L. appendiculata, L. spicata and T. 88 macrostachys have nondeep simple MPD (Baskin and Baskin 2005; Baskin et al. 2005). 4 https://mc06.manuscriptcentral.com/botany-pubs Page 5 of 19 Botany 89 Actually, fresh seeds of C. fauriei, C. hawaiiensis, C. kakeana and C. angustifolia have 90 conditional MPD because the level of PD in the seeds is nondeep and seeds exhibit an increase in 91 range of temperatures for germination as PD is broken. In these species, the embryo grew and 92 seeds germinated to a high percentage at 25/15 in 4 weeks, but after 8-12 weeks seeds gained the 93 ability to germinate to high percentages at 20/10 and 15/6°C. It is well known that seeds with 94 the nondeep level of PD may exhibit an increase in the range of temperatures (or other 95 conditions) at which they can germinate to a high percentage. Thus, dormancy break in most 96 seeds with PD occurs along a dormancy continuum that starts at ≤ 1.0 (seeds dormant = 1.0 and 97 seeds conditionally dormant <1.0 but >0) and ends with 0.0 (seeds nondormant). Seeds along the 98 continuum between <1.0 and >0.0 are in conditional dormancy (Soltani et al. 2017). Draft 99 Seeds of various species of Campanulaceae, including 131 taxa [of Campanulaceae] from 100 around the world (Koutsovoulou et al. 2014), nine species of Campanula from Mt Olympos in 101 Greece (Blionis and Vokou 2005), Campanula fragilis subsp. cavolinii (Frattaroli et al. 2013), C. 102 glomerata (Gülbağ and Özzambak 2017), C. uniflora (Aegisdóttir and Thórhallsdóttir 2006), 103 Jasione crispa (Giménez-Benavides et al. 2005), Lobelia inflata (Muenscher 1936; Baskin and 104 Baskin 1992), Lobelia spp. from Australia (Fraser 1931; Warcup 1988) and Physoplexis comosa 105 (Cerabolinin et al. 2004), have been investigated with regard to the effect of dormancy-breaking 106 treatments and/or effect of incubation temperatures and/or light-dark on germination. Nikolaeva 107 et al. (1985) included 22 species of Campanulaceae (16 Campanula, 1 Codonopsis and 5 108 Phyteuma) in their reference book on seed dormancy and germination, and seeds of all of them 109 were assigned to PD. However, none of these studies gave any attention to pregermination size 110 of growth of the embryo; thus, it is not possible to classify the kind of dormancy in seeds of these 111 species with confidence. 5 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 6 of 19 112 The broad objective of the present study was to further classify the kind of dormancy and 113 the dormancy-breaking and germination requirements of the Campanulaceae in general and of 114 the Hawaiian lobelioids specifically. Studies were conducted on seeds of Cyanea kunthiana, 115 Delissea rhytidoperma, Lobelia grayana, L.
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