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Experimental Evaluation of Differences in Plastic Phenotypes Between Cardamine Fallax and C. Occulta: Effects of Seasonality on Phenology and Gross Morphology

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Experimental Evaluation of Differences in Plastic Phenotypes Between Cardamine Fallax and C. Occulta: Effects of Seasonality on Phenology and Gross Morphology ISSN 1346-7565 Acta Phytotax. Geobot. 71 (1): 23–32 (2020) doi: 10.18942/apg.201912 Experimental Evaluation of Differences in Plastic Phenotypes between Cardamine fallax and C. occulta: Effects of Seasonality on Phenology and Gross Morphology 1 2, 3 1,* Mie N. HoNjo , Karol MarHold aNd HirosHi KudoH 1Center for Ecological Research, Kyoto University, Hirano 2-509-3, Otsu, Shiga 520-2113, Japan. *[email protected] (author for correspondence); 2Institute of Botany, Plant Science and Biodiversity Centre, Slovak Academy of Sciences, Dúbravská cesta 9, SK-845 23 Bratislava, Slovak Republic; 3Department of Botany, Faculty of Science, Charles University, Benátská 2, CZ-128 01 Praha 2, Czech Republic Phenological responses in species of Cardamine are often accompanied by morphological changes that result in disagreement among researchers about the taxonomic rank and status of a particular taxon. The gross morphology of two closely related eastern Asian species, Cardamine fallax (O. E. Schulz) Nakai and C. occulta Hornem., was compared by growing plants under controlled photoperiod and vernaliza- tion conditions. Response to photoperiod and vernalization in C. fallax and C. occulta explained differ- ences in phenology between the two species under natural conditions. The gross morphology was dis- tinctive between the two species grown under the same conditions, but overlapped when C. fallax was grown in the spring photoperiod-temperature regime and C. occulta grown in the autumn environmental regime. Cardamine fallax is distinct from C. occulta in gross morphology when seasonality in flowering time is taken into account. The findings support the distinction between C. fallax and C. occulta. A sur- vey of herbarium specimens revealed the upper cauline leaves of C. fallax to be moderately or densely hairy, while those of C. occulta were glabrous or sparsely hairy. Key words: Brassicaceae, Cardamine fallax, C. occulta, chilling treatments, diagnostic characters, flow- ering phenology, gross morphology, long-day plants, photoperiod, vernalization Cardamine L. (Brassicaceae) with more than species (Kim et al. 2009). Changing these factors 200 species, is one of the largest genera in the not only changes flowering time, but may also family (Lihová & Marhold 2006, Marhold et al. modify gross morphology of some annual species 2018). Differences in gross morphology, such as of Cardamine so that the phenotype is highly de- growth form and leaf shape, is often used to dis- pendent on seasonality (Kudoh et al. 1993, 1995, tinguish between species of Cardamine, especial- 1996). Species of Cardamine form rosettes after ly between closely related taxa that share flower germination. Prior to flowering, the internodes of and fruit morphology (e.g., Marhold 1996, Kučera the upper stem elongate to form the flower stalk et al. 2010, Šlenker et al. 2018). Gross morpholo- while the internodes of the lower stem near the gy is often plastic, making correct interpretation rosette exhibit minimal growth. At anthesis, the of variation important for taxonomic diagnosis plants have both rosette and cauline leaves. Cau- (Kudoh et al. 1993). It has been reported that line leaves are therefore only present during the many species of Brassicaceae, including species reproductive season. The number, shape and dis- of Cardamine, have flowering times dependent section of the cauline leaves are often used as di- on photoperiod and degree of exposure to pro- agnostic characteristics. The rosette and cauline longed cold (vernalization). Long daylight hours leaves are imparipinnate in Brassicaceae. There- and vernalization promote flowering in many fore, gross morphology in Cardamine is charac- 24 Acta Phytotax. Geobot. Vol. 71 Table 1. Population codes, localities and phenology-related habitat environments of Cardamine fallax and C. occulta popula- tions used in this study. Species Population codes Locality Phenology-related habitat environments C. fallax KM (Kyoto Pref., Montane habitat) Kamakura, Kameoka-shi, alt. ca. Densely covered by kudzu-vine (Pueraria lobata) during 300 m summer C. fallax Inamura, Kamiichi-machi, Shaded by shrubs during summer; covered with snow TM (Toyama Pref., Montane habitat) Nakaniikawa-gun, alt. ca. 200 m during winter C. occulta KP (Kyoto Pref., Paddy field) Iwakura, Sakyo-ku, Kyoto-shi, alt. Submerged from May to August; plowed in late autumn ca. 100 m C. occulta TP (Toyama Pref., Paddy field) Kamijima, Namericawa-shi, alt. Submerged from May to August; covered with snow ca. 15 m during winter terized by patterns of stem elongation and branch- phylogeny, and Marhold et al. (2016) determined ing and the shape of the leaflets or sections of pin- the correct name to be C. occulta. While C. flex- nate leaves. uosa is tetraploid, C. occulta is octoploid. They Cardamine fallax (O. E. Schulz) Nakai of Ja- have distinct allopolyploid origins with different pan, Korea, and China (Marhold et al. 2007) was combinations of diploid parental species originally described as C. flexuosa With. subsp. (Mandáková et al. 2014, 2019). Lack of agree- fallax O. E. Schulz from Japan, and recognized as ment on the taxonomic rank and status of C. fal- such by Kitamura (1961) and Kimata (1983). It lax, therefore, is attributable to the close similar- was recognized as a distinct species by Kitagawa ity in gross morphology with C. occulta. (1982) and Kudoh et al. (1993) or as a variety of We compared the morphology of two closely C. flexuosa by Ohwi (1972, 1984), Lee (1996), related eastern Asian annual and biennial spe- Cheo et al. (1987). In the Flora of China (Zhou et cies, C. fallax and C. occulta, by growing them al. 2001) and Flora of Japan (Al-Shehbaz et al. under different vernalization and photoperiod re- 2006), it was placed in synonymy under C. parvi- gimes. Our objective was to determine the re- flora L. Based on an evaluation of the original sponse of C. fallax to photoperiod and vernaliza- materials, Marhold et al. (2007) concluded that it tion. The flowering season of C. fallax in May is should be treated as a species distinct from C. approximately one month later than in C. occulta parviflora and C. flexuosa. (Kudoh et al. 1993). We wanted to determine if Cardamine occulta Hornem. was described photoperiod and vernalization in C. fallax ex- based on material that originated from China and plain the differences in phenology between them. was grown in the University of Copenhagen Bo- The second objective was to determine if varia- tanical Garden (Hornemann 1819). The name has tion in gross morphology is distinct or to what been treated as a synonym of C. flexuosa, but it extent it overlaps with C. occulta under different has recently proven to represent a distinct taxon photoperiods and vernalization conditions. We that consists of Asian populations that had been also surveyed herbarium specimens to evaluate considered to be C. flexuosa (Marhold et al. seasonality in gross morphology of the two taxa. 2016). Cardamine flexuosa With. was described Based on our conclusions we provide a key to based on plants in England, and both the Euro- separate C. fallax from C. occulta. pean and Asian populations had been treated as a single species with a pan-Eurasian distribution (Jalas & Suominen 1994, Zhou et al. 2001, Al- Materials and Methods Shehbaz et al. 2006). Lihová et al. (2006) sug- gested that the eastern Asian populations belong Plant materials to a distinct taxon from C. flexuosa based on cp- We chose two populations each of Cardamine DNA (trnL-trnF region) and the nrDNA (ITS) fallax and C. occulta; one from Toyama Prefec- February 2020 HoNjo & al. — Plastic Phenotypes of Cardamine fallax and C. occulta 25 ture and the other from Kyoto Prefecture (Ta- ble 1, Fig. 1). These are the same populations used by Kudoh et al. (1993) to describe pheno- typic variation under field conditions. Seeds were collected from 12 plants for each population, from Cardamine occulta in April and from and C. fallax in May. The populations were located in different habitats and climatic zones, the Toyama montane population of C. fallax (TM) and the Toyama paddy field population of C. occulta (TP), on the Japan Sea side of Honshu, which is covered by deep snow in winter. The snow pro- vides milder winter temperatures, thermal insu- lation and dark moist conditions on the ground surface. In contrast, the Kyoto montane popula- tion of C. fallax (KM) and the Kyoto paddy field population of C. occulta (KP) are on the Pacific side of Honshu and exposed to dry, freezing con- ditions during the winter. Experimental design Parts of the results of the experiments were Fig. 1. Four sampling sites in this study. Toyama montane published previously for the TP and KP popula- (TM) and Kyoto montane (KM) populations of Carda- tions of C. occulta (as C. flexuosa in Kudoh et al. mine fallax and Toyama paddy field (TP) and Kyoto pad- 1995). In the current study, we reanalyzed data dy field (KP) populations of C. occulta. for C. occulta and added the results of unpub- lished data on C. fallax. Growth experiments were conducted under the same conditions simul- °C/15 °C (day/night). Non-chilled plants were taneously for the two species. Seeds were stored transferred to growth cabinets one week after be- at room temperature until they were used in the ing transplanted into pots. We determined the growth experiments. In late August, the seeds photosynthetically active radiation (PAR) in the were sown and germinated in the greenhouse. growth cabinets, ca. 230 ~mol m-2 s-1 on average Two weeks after sowing, eight to ten seedlings at the surface of the pots, by use of a data logger from each parental plant (12 plants /population) (LI-1000, Li-Cor; USA) with LI-190SA sensor were transplanted into plastic pots and cultivated (Li-Cor). Light was supplied by a combination of under four conditions; chilling + long day (C-L), 22, 80-W fluorescent lamps (Toshiba), 9, 400-W non-chilling + long day (NC-L), chilling + short extra high pressure mercury lamps (metal-halide, day (C-S), non-chilling + short day (NC-S).
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