Breaking seasonal limitation: year-round sporogenesis in the brown alga Laminaria saccharina by blocking the transport of putative sporulation inhibitors
Introduction
Seaweeds in nature often demonstrate a pronounced seasonal growth and reproduction pattern, with a period of rapid growth in spring and formation of sporangia in late autumn and winter (Kain, 1979, Kain, 1991, Lüning, 1990, Lüning, 1993). The commercial cultivation of Laminaria depends on seasonal availability of sorus-bearing sporophytes from which gametophytes and subsequently sporelings can be produced. In Laminaria culture, release of zoospores and cultivation of juvenile sporophytes are normally performed once per year due to seasonal restriction of sorus availability in nature and, in several places, suitable seawater temperatures for open sea cultivation (Tseng et al., 1955, Perèz et al., 1992). As an alternative method to zoospore seeding, filamentous gametophytes were used to seed collectors for seedling production in some species of the Laminariales (Perèz et al., 1992, Ohno and Matsuoka, 1993, Pang et al., 1997), but current commercial Laminaria cultivation uses mostly the zoospore method (Ohno and Critchley, 1997).
Year-round induction of sporogenesis in Laminaria has now become technically feasible due to recent evidence for putative sporulation inhibiting factor(s) produced by the meristematic base of the blade (Buchholz and Lüning, 1999). In Laminaria digitata, blade discs isolated at some distance from the blade base and cultivated at 8, 12 or 16 h light/day formed sorus 7–12 weeks later, while blade discs isolated from or near to the meristematic blade base did not form sorus (Buchholz and Lüning, 1999). This suggests that the basal, actively growing part of the laminarian frond is the source of inhibitors for sporangium formation that move in distal direction and keep the young frond free of sporangia (sorus) during the season of rapid growth (Buchholz and Lüning, 1999, Lüning et al., 2000). Early sorus formation in isolated blade discs was also reported for Laminaria japonica by Mizuta et al. (1999a). Sporulation inhibiting substances were earlier detected by Stratmann et al. (1996) as a glycoprotein and a nonprotein substance with a very low apparent molecular mass in the green alga Ulva sp., after the observation of promoted reproductive maturing in isolated blade discs (Nilsen and Nordby, 1975).
In Laminariales, the view of the actively growing meristematic blade base as a source of distally moving sporulation inhibitor(s) was supported by another method for meristem separation, namely by cutting a hole into the actively growing thallus of L. digitata, i.e., mechanically blocking the pathway of the hypothesized sporulation-inhibiting factor(s) resulting in sorus formation along the distal margin of the hole after 5–10 weeks (Lüning et al., 2000).
Laminaria saccharina is a photoperiodic, short-day (SD) reproductive kelp forming sorus in the field only from October to January and, in the laboratory, not in long days (LD) or in a night-break regime (Lüning, 1988). Similarly to Laminaria digitata, distal blade discs of L. saccharina isolated from field plants in June formed sorus 7 weeks later by end of July, but only at 8 h, not at 16 h light/day (Buchholz and Lüning, 1999). This alga thus requires not only the separation of blade discs from the meristem, but in addition a short-day treatment for sorus formation in summer. The principal goal of the present investigation was to try out, in more details, the possibility of having year-round induction of sporogenesis in L. saccharina under various pre- and post-culture conditions and to try to achieve year-round production of sporelings independent of season.
Section snippets
Algal material
Sporophytes of L. saccharina (L.) Lamour used for induction of sporogenesis were either collected in the field (Helgoland, North Sea, Germany) or grown in greenhouse tanks. Tank-grown sporophytes had been derived from spores released from either field-collected mature sporophytes or laboratory-induced sorus. In the latter case, the indicated age of the sporophytes refers to the culturing period from the date of spore release to the start date of experimental treatment.
Outdoor tank cultivation system in a greenhouse (system 1)
The culture of either
Induction of sporogenesis in blade fragments or behind transverse cuts
The fast growing basal meristematic portion of a blade of L. saccharina and the stipe and haptera were removed and the subsequent medium portion was cultivated as an “induction fragment” (Fig. 1A) in a short-day (SD) tank (8 h light/day) in a greenhouse. Under SD condition, sorus formation in blade fragments occurred approximately 20–35 days later (Fig. 1B and C; Table 1, expts. 1–4). Intact control plants in the same tank did not form sorus at the time indicated for first observation of sorus.
Gradient of sporulation inhibiting factors and the direction of transport
The finding that sorus was only induced when a sufficiently long transverse cut was made in the frond points to the possibility that the inhibitor(s) originating from the meristematic blade base travel mainly in longitudinal pathway and converge laterally towards the medium section of the blade preventing sorus formation in this way, if the transverse cut was too short. Another sign of lateral convergence was the candle flame-like shape of the sorus behind a long cut, probably mirroring by its
Acknowledgement
The authors thank Petra Kadel for technical help. All experiments were performed at the Wattenmeerstation Sylt, Alfred Wegener Institute for Polar and Marine Research (AWI), Germany. This work was financially supported by the EU project Seapura (Contract Q5RS-2000-31334. Website: http://www.seapura.com).
References (26)
- et al.
Early embryo development in Fucus distichus is auxin sensitive
Plant Physiol.
(2002) - et al.
Tank cultivation of Irish Moss, Chondrus crispus
Bot. Mar.
(1985) - et al.
Isolated, distal frond discs of the brown alga Laminaria digitata form sorus, but not discs near to the meristematic transition zone
J. Appl. Phycol.
(1999) - et al.
Evolutionary patterns in auxin action
Plant Mol. Biol.
(2002) - et al.
Breeding of the new variety, Danhai No. 1 of Laminaria japonica by using a female haploid clone of the kelp
J. Shandong Col. Oceanol.
(1983) A view of the genus Laminaria
Oceanogr. Mar. Biol. Ann. Rev.
(1979)Cultivation of attached seaweeds
The growth and death of the Macrocystis sporophyte (Phaeophyceae Laminariales)
Phycologia
(1978)Photoperiodic control of sorus formation in the brown alga Laminaria saccharina
Mar. Ecol., Prog. Ser.
(1988)Circannual growth rhythm in a brown alga, Pterygophora californica
Bot. Acta
(1991)
Environmental and internal control of seasonal growth in seaweeds
Hydrobiologia
Mass cultivation of seaweeds: current aspects and approaches
J. Appl. Phycol.
Seaweeds. Their Environment, Biogeography, and Ecophysiology
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