Porphyra – the Economic Seaweed As a New Experimental System

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3. Velayudhan, K. C., Muralidharan, V. K. 10. Sharma, R. K., Misra, B. P., Sarma, T. C., Received 9 June 2000; revised accepted 7 and Amalaraj, V. A., J. Econ. Tax. Bot., Bordoloe, A. K., Pathak, M. G. and Le- October 2002 1990, 14, 579–582. clerq, P. A., ibid, 1997, 9, 589– 4. Baruah, P. and Sarma, G. C., ibid, 1987, 592. 11, 71–76. 11. Verma, V. P. S., Shiva, M. P., Suki, R. K. 5. McCarron, M., Mills, A. J., Whittaker, and Subramanyan, I. V., Indian For., SAKUNTALA BEHURA* D., Sunny, T. P. and Verghese, J., Fla- 1978, 104, 846. S. SAHOO † vour Fragrance J., 1995, 10, 355–357. 12. Panda, R. and Panda, H., ibid, 1987, 113, V. K. SRIVASTAVA 6. Zwaving, J. H. and Bos, R., ibid, 1992, 7, 434–440. 19–22. 13. Dung, N. X., Truong, P. X., Ky, T. Pham Aromatic and Medicinal Plants Division, 7. Dung, N. X., Tuyet, N. T. B. and Le- and Leclerq, P. A., J. Essent. Oil Res., Regional Research Laboratory, clercq, P. A., J. Essent. Oil Res., 1995, 7, 1997, 9, 677–681. Bhubaneswar 751 013, India 701–703. †Germplasm Evaluation Division, 8. Ramachandraiah, O. S., Azeemoddin, G. National Bureau of Plant Genetic and Krishnama Charyulu, J., Indian Per- ACKNOWLEDGEMENTS. We thank the fum., 1998, 42, 124–127. Council of Scientific and Industrial Research Resources, 9. Choudhury, S. N., Ghosh, A. C., Saikia, for the Research Associate fellowship and Pusa Campus, M., Choudhury, M. and Leclercq, P. A., Prof. H. S. Ray, Director, RRL for encour- New Delhi 110 012, India J. Essent. Oil Res., 1996, 8, 633–638. agement during the work. *For correspondence

Porphyra – the economic seaweed as a new experimental system

Marine algae, popularly known as sea- found that the plant has much more poten- completely revolutionized the Porphyra weeds, are sources of food, fodder, ferti- tial and can be used as an experimental industry in Japan and subsequently lizer, medicine and chemicals1. World system like Arabidopsis thaliana in the throughout Asia. trade in seaweed and its products was val- higher plants, some aspects of which are Porphyra reproduces by both sexual and ued at US $ 50 million in 1970, US $ 250 discussed here. asexual modes of reproduction. In sexual million in 1990 and US $ 6.2 billion in Nearly 133 species of Porphyra have reproduction, certain mature vegetative 1999 (refs 1 and 2). About 20,000 marine been reported from all over the world, cells of the thallus get differentiated into algae species are distributed throughout which includes 28 species from Japan, 30 carpogonia, and others on the same or the world, out of which only 221 species from North Atlantic coasts of Europe and different thallus get differentiated into are utilized commercially. These include America and 27 species from the Paci- colourless spermatangia. After fertili- 145 species for food and 110 species for fic coast of Canada and United States8. zation, the carpogonia divides to form phycocolloid production1. Porphyra (Ban- Although seven species have been reported packets of spores called zygotospores giales, Rhodophyta) popularly known as from the Indian coast, these are not being (carpospores). After release, the zygoto- ‘Nori’ in Japan, ‘Kim’ in Korea and ‘Zicai’ exploited commercially9. The genus Por- spores usually germinate unipolarly to in China has an annual value of over US phyra has a simple morphology. The produce the filamentous conchocelis $ 1.8 billion3. Porphyra is primarily used plants are either round, round to ovate, phase. The conchocelis can survive in as food, wrapped around the Japanese obovate, linear or linear lanceolate (Figure adverse environmental conditions, but delicacy ‘Sushi’ which consists of roas- 1 a–d). Individuals can also have blades give rise to conchosporangia and concho- ted blades, raw fish, rice and other ingre- that may be divided into male and female spores under suitable conditions. The con- dients. The alga is not only delicious but sections10, or have a sectored morphology11. chospores germinate by bipolar modes to also contains high levels of protein (25– The plants can grow from 5 to 35 cm in give rise to young chimeric thalli, thus 50%), vitamins (higher vitamin C than in length. The thalli are either one or two completing the life cycle (Figure 2 ). oranges), trace minerals and dietary fibres4. cells thick, and each cell has one or two In asexual reproduction, the vegetative The plant contains nearly 17 types of stellate chloroplasts with a pyrenoid. cells in some species directly form the free amino acids, including taurine which Porphyra has a heteromorphic life cycle spores called archeospores which can controls blood cholesterol levels5. The with an alternation between a macroscopic directly germinate to form the thallus13 alga is a preferred source of the red pig- foliose thallus which is the gametophytic (Figure 1 i). Recently, it has been found ment r-phycoerythrin, which is utilized phase, and a filamentous sporophyte called that besides these two modes of repro- as a fluorescent ‘tag’ in the medical diag- conchocelis phase. This diploid concho- duction, Porphyra also reproduces by nostic industry6. Porphyra has been cul- celis phase in the life cycle was earlier endosporangia or endospores which ulti- tivated for the past hundred years in Japan thought to be Conchocelis rosea, a shell- mately give rise to the thallus14. and today it is one of the largest aquacul- boring organism. However, it was Drew Different stages in the life cycle can be ture industries in Japan, Korea and in 1949 who demonstrated in culture that manipulated both in the laboratory as China6. Because of its economic impor- P. umbilicalis (L.) Kütz had a diploid well as on an industrial scale. Large-scale tance and other health benefits, Porphyra conchocelis phase12. Until this landmark conchocelis are being cultured in suitable cultivation is now being expanded to work concholeis was considered as an environmental conditions by different Nori other countries7. Recently, it has been independent organism. These findings companies. Massive amount of con-

CURRENT SCIENCE, VOL. 83, NO. 11, 10 DECEMBER 2002 1313 SCIENTIFIC CORRESPONDENCE

Figure 1. a–k. Porphyra sp. Morphology and development. a, Field material of Porphyra kanyakumariensis from Kerala, India; b, Cultured P. katadai var. hemiphylla from Qingdao, P.R. China; c, Field material of P. yezoensis from Qingdao, P.R. China; d, Field material of P. vietna- mensis from Goa, India; e–h, Different stages of conchospore development, Scale bars = 25 mm; i, Release of archeospores from the mature thallus. Several young thalli were formed from these spores. Scale bar = 50 mm; j, Massive conchospores released from conchosporangia. Scale bar = 25 mm; and k, Large number of young and homogenous thalli in culture after the germination of conchospores. Scale bar = 100 mm.

1314 CURRENT SCIENCE, VOL. 83, NO. 11, 10 DECEMBER 2002 SCIENTIFIC CORRESPONDENCE chospores can be released (Figure 1 j), does not take place under these culture under different environmental conditions. seeded onto the nori nets and subse- conditions. However, when the conchos- A number of studies reveal that each quently can be transplanted into the sea porangia are transferred from 20 to 15°C, stage in the life cycle of Porphyra is for large-scale cultivation. Traditionally, the conchospores get released. While species-specific and dependent on light, a large amount of shells (1–2 ´ 106 spermatia get released at 10 and 15°C, temperature and photoperiod17– 20. shells) are required to maintain and grow zygotospores get liberated only at 15°C An emerging problem of coastal conchocelis on a commercial scale. This (ref. 15). In P. leucosticta the growth of mariculture activities is the significant occupies an enormous amount of space conchocelis was twice as fast at 15°C in loading of inorganic nutrients into local and the methods are labour-intensive. short-day condition compared to the day- waters. Nutrient enrichment from fish Recent research has shown that free con- neutral and long-day condition, whereas and shrimp farming is equivalent to that chocelis can be maintained in a large- the gametophytic thalli grew well at of municipal sewage. So it is important scale inside bioreactors. 15°C in short-day condition. When con- to remove the excessive nitrogen and Although several studies have been chocelis were transferred from the high phosphorus from the aquaculture systems made on different aspects of Porphyra, light intensity to low light intensity, con- in a sustainable way. Recently, it has light, temperature and photoperiod play a chosporangia were found in 1–2 weeks, been found that different species of Por- major role by which its life cycle can be but conchospores did not liberate up to phyra can be effectively used as nutrient manipulated. one month. The life cycle was completed scrubbers21,22. Because of its rapid nutri- It has been found that temperature and in the laboratory in 2–3 months16. In a ent-removal capacity from the environ- photoperiod play a major role in each similar study in P. leucostica from USA, ment, Porphyra is now being planned for stage of the life history of Porphyra. For the present authors found that the life use in integrated finfish culture23. example, in P. dentata and P. pseudolin- cycle can be completed in less than one As mentioned earlier, Porphyra pro- earis, the growth and maturation of con- month at 15°C 12:12 L:D conditions duces three different kinds of spores: chocelis occurred between 10 and 25°C. (unpublished). This suggests that the same archeospores, zygotospores and concho- Interestingly, conchospore liberation species can have different behaviour spores. The archeospores are haploid,

Figure 2. Life history of Porphyra showing different stages of development.

CURRENT SCIENCE, VOL. 83, NO. 11, 10 DECEMBER 2002 1315 SCIENTIFIC CORRESPONDENCE directly germinate and subsequently teria, while the remaining 60% are 21. Kraemer, G. P. and Yarish C., J. Appl. divide to give rise to the thallus (Figure novel30. Phycol., 1999, 11, 473–477. 1 i). In contrast, the zygotospores and In conclusion, we think Porphyra is 22. Chopin, T. et al., J. Phycol., 2001, 37, conchospores are diploid, while zygoto- one of the best marine organisms for 975–986. 23. Kraemer, G. P., Yarish, C. and Carmona, spores give rise to conchocelis (sporo- both applied and basic research. How- R., Abstracts Algae 2002, p. 48. phyte), the conchospores undergo meiosis ever, more research is needed to unravel 24. Tseng, C. K. and Sun, A., Bot. Mar., to give rise to haploid thalli that may be several other aspects of the biology of 1989, 32, 1–8. 11 considered chimeric individuals (Figure Porphyra. 25. Wilkes, R. J., Yarish, C. and Mitman,

1 g, h). One can easily study each stage G. G., Algae, 1999, 14, 219–222. of development under a microscope with- 1. Sahoo, Dinabandhu, Farming the Ocean- 26. Chen, L. C. M., Bot. Mar., 1986, 26, out much difficulty (Figure 1 e–h). Since Seaweeds Cultivation and Utilization, 435–439. the thallus is either single-layered or Aravali Books International, New Delhi, 27. Chen, L. C. M., McCracken, I. R. and double-layered, it is a good material for 2000, p. 44. Xie, Z. K., ibid, 1995, 38, 335–338. cytological studies. One can see 2–5 pairs 2. Hanisak, M. D., World Aquacult., 1998, 28. Fujita, Y. and Saito, M., Hydrobiologia, of chromosomes at different stages of 29, 18–21. 1990, 204/205, 161–166. 29. Chen, L. M., Bot. Mar., 1987, 30, 399–403. mitosis and meiosis24,25. Protoplast iso- 3. Yarish, C., Chopin, T., Wilkes, R., Mathieson, Fei, X. G. and Lu, S., Bull. 30. Asamizu, E., Nakajima, M., Nakamura, lation and fusion amongst various spe- Y., Nikaido, I., Kitade, Y., Saga, N. and cies of Porphyra have been achieved, Aquacult. Assoc. Can., 1999, 1, 11–17. 4. Noda, H, J. Appl. Phycol., 1993, 5, 255– Tabata, S., Abstracts Algae 2002, p. 26. including intergeneric somatic hybridi- 258. zation26–28. Morphogenetic studies have ACKNOWLEDGEMENTS. We thank Dr 5. Tsujii, K., Kchikawa, T., Matusuura, Y. Sheryl Miller for helping us in various ways also been carried out from the Porphyra and Kawamura, M., Sulphur Amino 29 during the preparation of the manuscript. D.S. protoplast . Acids, 1983, 6, 239–248. thanks Department of Biotechnology, Govern- Porphyra has recently been gaining 6. Mumford, T. F. and Miura, A., in Algae ment of India, New Delhi for the award of momentum as a model plant for basic and Human Affairs (eds Lemby, C. A. Overseas Biotechnology Associateship. X.T. and applied studies in plant science. There and Walland, J. R.), Cambridge Univ. thanks National Natural Science Foundation are several advantages to study develop- Press, Cambridge, 1988, pp. 87–117. of China for financial support. C.Y. acknow- ment, physiology, cytology, genetics and 7. Levine, I. A., Bull. Aquacult. Assoc. ledges support of the State of Connecticut genomics. For example, establishment of Can., 1999, 1, 31–33. Critical Technology Programme, USA, C.T. 8. Yoshida, T., Notoya, M., Kikuchi, N. and several pure lines (Figure 1 k), the small Seagrant College Programme and NOAA’s Miyata, M., Nat. Hist. Res. (Spec. Issue), National Marine Aquaculture Initiative, USA. genome size which is estimated to be 1997, 3, 5–18. 8 2.6 ´ 10 base pairs consisting of three 9. Sahoo, Dinabandhu, Nivedita and Received 18 September 2002; revised accepted chromosomes and short generation time Debasish, Seaweeds of Indian Coast, 3 October 2002 (1–3 months) are suitable for genetic APH Publishing Corporation, New Delhi, analysis. To understand the whole genetic 2001, p. 283 DINABANDHU SAHOO system in red algae, large-scale expressed 10. Tang, X. R. and Fei, X. G., Ocean Lim- †, XIAORONG TANG * sequence tag (EST) analysis of P. yezo- nol. Sin., 1999, 30, 180–185 (In Chinese ,# CHARLES YARISH* ensis has been initiated. Normalized and with English abstract). 11. Mitman, G. G. and van der Meer, J. P., size-selected cDNA libraries were gene- Marine Biotechnology Laboratory, J. Phycol., 1994, 30, 147–159. rated from both gametophytic and sporo- 12. Drew, K. M., Nature, 1949, 164, 748–751. Department of Botany, phytic stages of P. yezoensis Ueda (strain 13. Nelson, W. A., Brodie, J. and Guiry, University of Delhi, TU-1), and single-pass sequencing was M. D., J. Appl. Phycol., 1999, 11, 407–410. Delhi 110 007, India † performed from the 5¢-end of each cDNA 14. Nelson, W. A. and Knight, G. A., Bot. College of Marine Life Sciences, clone. As of April 2002, 10,154 and Mar., 1995, 38, 17–20. Ocean University of Qingdao, 10,625 5¢-end ESTs were established 15. Nam-Gil, K., Hydrobiologia, 1999, Qingdao 266003, from gametophytic and sporophytic stages 398/399, 127–135. People’s Republic of China respectively. These EST sequences were 16. Sidirelli-Wolf, M., Bot. Mar., 1992, 35, *Marine Biotechnology Laboratory, clustered into 4896 non-redundant 251–257. Department of Ecology and Evolutionary 17. Katz, S., Kizner, Z., Dubinsky, Z. and groups. Database search of the 4896 non- Biology, Friedlander, M., J. Appl. Phycol., 2000, redundant ESTs by BLAST algorithm 12, 535–542. University of Connecticut, showed that approximately 40% have 18. Orfandis, S., Bot. Mar., 2001, 44, 533–539. Stamford, similarity to those of registered genes 19. Avila, M., Santelices, B. and McLachlan, Connecticut 06901-2315, USA # from various organisms, including higher J., Can. J. Bot., 1986, 64, 1867–1872. For correspondence. plants, mammals, yeast and cyanobac- 20. Oohusa, T., Bot. Mar., 1980, 23, 1–5. e-mail: [email protected]

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