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Temperature Promoting the Asexual Life Cycle Program in Bangia Fuscopurpurea (Bangiales, Rhodophyta) from Esashi in the Hokkaido Island, Japan

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Temperature Promoting the Asexual Life Cycle Program in Bangia Fuscopurpurea (Bangiales, Rhodophyta) from Esashi in the Hokkaido Island, Japan Algal Resources (2018) 11：25-32 Temperature promoting the asexual life cycle program in Bangia fuscopurpurea (Bangiales, Rhodophyta) from Esashi in the Hokkaido Island, Japan Koji MIKAMI1 * and Ikuya KISHIMOTO2 Abstract : In the asexual life cycle of the marine red seaweed Bangia fuscopurpurea gametophytic thalli produce multiple monospores that develop into thalli as clones. We investigated the effects of heat stress on the production and release of monospores in B. fuscopurpurea from Esashi, in northern Hokkaido Island of Japan. Non-lethal high tem- peratures of 25℃ and 28℃ strongly promoted monospore discharge, whereas no spore release was observed at 30℃, the limiting growth temperature of Esashi B. fuscopurpurea. These findings differed from previous reports using B. fuscopurpurea collected at Fukaura, the northern Japan, and at the Fujan province of southern China, for which growth and monospore release were observed at 30℃. Thus, the temperature range promoting asex- ual propagation with monospore discharge in B. fuscopurpurea varies and appears to be unrelated to the thermal conditions of harvesting areas. Since each B. fuscopurpurea strain had a unique upper-limit temperature for survival and release of monospores was accelerated under non-lethal high temperature conditions, the temperature range ena- bling the asexual life cycle program seems to be restricted by the degree of heat stress tolerance of the B. fuscopurpurea strains themselves. Keywords : asexual propagation, Bangia fuscopurpurea, heat stress, life cycle Introduction growth and development as a strategy for stress acclimation (Potters et al. 2007). Environmental fluctuation is a major factor As opposed to terrestrial plants, seaweeds are influencing the growth, development and sur- aquatic multicellular sessile organisms that ex- vival of terrestrial plants (Cramer et al. 2011; ist at the intertidal and subtidal zones. The Kumar et al. 2012; Pandey et al. 2017). For conditions in the intertidal zone especially ex- instance, an increase in the air temperature hibit drastic changes at both daily and yearly surrounding plants can lead to physiological scales (Rawlings 1999; Helmuth and Hofmann defects especially in reproductive processes 2001; Eckersley and Scrosati, 2012). Thus, sea- (Barnabas et al. 2008; Zinn et al. 2010; Hartfield weeds also are exposed to temperature fluctua- and Prueger 2015). However, stress-tolerance tions that influence their growth and develop- mechanisms can allow plants to acclimate to ment (Wiencke and Dieck 1989; Dudgeen et al. such environmental stresses (Nakashima et al. 1995; Ku bler and Davison 1993, 1995; Nejrup et 2014; Rejeb et al. 2014; Zhu 2016; Sade et al. 2017; al. 2013; De Silva and Asaeda 2017; Martins et Vishwakarma et al. 2017). Indeed, abiotic stres- al. 2017; Mikami et al. 2018; for review, Agrawal ses often bring about modulations of morpho- 2012; Singh and Singh 2015). Temperature is one genic responses, with inhibition or promotion of ofthemostvariablefactorsintheirenviron- 1 Faculty of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-8611, Japan 2 Graduate school of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-8611, Japan ＊Corresponding author : Tel / fax: +81-138-40-8899, e-mail: [email protected] 25 Koji MIKAMI and Ikuya KISHIMOTO ment, and seaweeds have acquired tolerance 2017). The asexual propagation in Bangiales has against temperature changes (Andersen et al. been studied mainly in Pyropia yezoensis and 2013; Smolina et al. 2016). However, it is un- Banga fuscopurpurea to date. In P. yezoensis, clear how heat stress-tolerance is regulated, which is a major cultivated species for nori although effects of temperature changes on production in Japan (Blouin et al. 2011), the compositions of amino acids and membrane production and release of monospores is accel- fatty acids have been demonstrated (Mikami et erated by a reduction in the extracellular al. 2011, 2018; de Costa et al. 2018; Song et al. calcium ion concentration (Takahashi et al. 2018), and transcriptional analyses have identi- 2010) and treatment of thalli with hydrogen fied a number of genes whose expression is up- peroxide (Takahashi and Mikami 2017). In or down-regulated by heat stress in various addition, asexual reproduction in thalli of P. seaweeds (Collen et al. 2007; Heinrich et al. 2012; yezoensis is also accelerated by irradiance (Li Choi et al. 2013; Im et al. 2015; Sun et al. 2015; 1984) and fragmentation associated with woun- Fan et al., 2017; Wang et al. 2018). ding (Hafting 1999). The effects of environmen- Seaweeds exhibit sexual reproduction with tal stresses on the asexual reproduction in B. isomorphic or heteromorphic diploid-haploid life fuscopurpurea have been examined only for cycle (Thornber 2006; Coelho et al. 2007; Cock et changes in temperature and photoperiod. These al. 2014; Liu et al. 2017). Among the Bangiales, studies indicated that heat stress stimulates the life cycle consists of a visible leafy thallus the formation and discharge of monospores and a microscopic filamentous conchocelis as a (Sommerfeild and Nichols 1973; Notoya and haploid gametophyte and a diploid sporophyte, Iijima 2003; Wang et al. 2008). Therefore, woun- respectively, both of which are multicellular and ding and heat stress might potentially act as live independently in different seasons of the triggers of the asexual life cycle program in year, and sexual reproduction is based on the Bangiales, suggesting that both biotic and abi- fertilization of male and female gametes pro- otic stresses are key regulators of both sexual duced in a gametophytic thallus to produce and asexual life cycle programs in red sea- carpospores that develop into a sporophytic weeds. conchocelis (Blouin et al. 2011; Mikami et al. Notoya and Iijima (2003) compared the opti- 2012; Takahashi and Mikami 2017). Since the mum temperature for growth and monospore rate of production of male and female gametes discharge and found differences in these pa- on gametophytes for sexual propagation is rameters for B. fuscopurpurea strains collected enhanced by increased temperature and photo- from Fukaura and Enoshima, located northern period (Kakinuma et al. 2006), it is possible that and central Japan, respectively. The Fukaura B. the sexual life cycle program is positively regu- fuscopurpurea was able to grow and release lated in part by heat stress in Bangiales, which monospores at 30℃,whereas25℃ was the would be similar to the green alga Volvox upper limit temperature for growth and mono- carteri (Kirk and Kirk 1986) and different from spore discharge for the Enoshima strain. Inter- the negative effects of heat stress on reproduc- estingly, B. fuscopurpurea from Fujan province tion in terrestrial plants (Barnaba s et al. 2008; in southern China was similar to the Fukaura Zinn et al. 2010; Hartfield and Prueger 2015). species [compare Notoya and Iijima (2003) and Therefore, effects of heat stress on the sexual Wang et al. (2008)]. These observations suggest reproductive process might differ between ter- that the prevailing temperature conditions in the restrial plants and algae. living areas do not correlate with the preferred As a remarkable characteristic, the life cycle temperature range for vegetative growth and of certain species of Pyropia, Porphyra, and the occurrence of asexual reproduction in B. Bangia in Bangiales includes an asexual pro- fuscupurpurea. gram via production of haploid neutral spores To address this possibility, we investigated or monospores from thalli (Blouin et al. 2011; whether B. fuscopurpurea collected at Esashi on Mikami et al. 2012; Takahashi and Mikami the northern Hokkaido Island of Japan exhibits 26 Temperature promoting the asexual life cycle program in Bangia fuscopurpurea (Bangiales, Rhodophyta) from Esashi in the Hokkaido Island, Japan difference in temperature range for survival and pores were determined daily for 7 days. monospore discharge compared to those col- To test viability, cells in thalli treated with lected in Fukaura, Enoshima, and Fujian. various temperatures for one to three weeks were visualized daily by staining with ESL Materials and Methods medium containing 0.01％ erythrosine (Wako Pure Chemical Industries, Japan). After stai- Algal material ning for 5 min at room temperature, thalli were Naturally growing B. fuscopurpurea gameto- gently rinsed with ESL medium to remove phytic thalli were collected at Esashi, Hokkaido, excess erythrosine and mounted on a slide with Japan on 14 May 2010. A clean single thallus ESL medium. Thalli were observed and photo- whose sex was unknown was cultured in graphed using an Olympus IX73 light micro- enriched sea life (ESL) medium (Kitade et al. scope equipped with an Olympus DP22 cam- 2002), which is made by dissolving commercially era, where cells stained by the dye were de- available SEALIFE powder (Marintech Co. Ltd., fined as dead cells. Viability was calculated by Japan) in distilled water (DW) with the addi- counting the living and dead cells using micro- tion of ESS２ solution, at 15℃ under irradiation graphs. of 60 mol m-2 s-1 provided by cool white fluo- The number of monospores discharged and rescent lamps (Neorumi super FL40SW, Mitsu- adheredonthebottomofa6well-microplate bishi, Japan) with a photo-period of 10 h light : with lid (Iwaki, Asahi Glass Co. Ltd., Japan) was 14 h dark. The medium was bubbled continu- counted daily for a week under the Olympus ously with filter-sterilized air and changed IX73 light
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