Porphyra: a marine crop shaped by stress Nicolas A. Blouin 1 , Juliet A. Brodie 2 , Arthur C. Grossman 3 , Pu Xu 4 and Susan H. Brawley 1 1 School of Marine Sciences, University of Maine, Orono, ME 04469, USA 2 Natural History Museum, Department of Botany, Cromwell Road, London, UK, SW7 5BD 3 Department of Plant Biology, Carnegie Institution, Stanford, CA 94305, USA 4 Department of Biology, Changshu Institute of Technology, Changshu 215500, China The marine red alga Porphyra is an important marine crop, worth US$1.3 billion per year. Cultivation research now includes farm ecology, breeding, strain conservation and new net-seeding technologies. The success of cultivation is due, in part, to the high stress tolerance of Porphyra. Many species of Porphyra lose 85–95% of their cellular water during the daytime low tide, when they are also exposed to high light and temperature stress. Antioxidant and mycosporine-like amino acid activities have been partially characterized in Porphyra, but, as we discuss here, the Porphyra umbilicalis genome project will further elucidate proteins associated with stress tolerance. Fur- thermore, phylogenomic and transcriptomic investiga- tions of Porphyra sensu lato could elucidate tradeoffs made during physiological acclimation and factors asso- ciated with life-history evolution in this ancient lineage. The organism Porphyra sensu lato belongs to the Bangiales (see Glossa- ry), the most genetically diverse order of the red algae [1]. The range of life histories in Porphyra probably reflects its ancient origin and long evolutionary history. Evidence supporting this comes from the filamentous Bangia-like fossil Bangiomorpha pubescens (found in the Hunting Formation, Somerset Isle, north Canada, dated to 1198  24 million years before present [Myr BP]) [2,3]. The oldest fossil evidence for eukaryotes is from 1780 to 1680 Myr BP [4], but B. pubescens is the oldest taxonomi- cally resolved eukaryotic fossil and appears to represent the oldest known case of sexual reproduction [5,6]. Identification of many Porphyra spp. is difficult because the 117 recognized species have similar morphology (http:// www.algaebase.org). The application of molecular techni- ques [7–12] has proved essential in revealing cryptic species [7], unrecognized cosmopolitan species [8], invasive species [9], ecotypes and genera. Molecular phylogenetic studies [7– 12], including a pending taxonomic revision of the Bangiales (Broom et al. unpublished), propose an increase in the number of genera, because Porphyra is a polyphyletic genus. The Joint Genome Institute (http://www.jgi.doe.gov/) is presently sequencing the complete nuclear genome of Por- phyra umbilicalis, which is a large eukaryotic genome (haploid genome 5–270 mb; reviewed in [13]). Extensive information is also being provided by the P. umbilicalis Genome Project on the proteins expressed in P. umbilicalis and the closely related Porphyra purpurea when they experience different stress and nutrient environments or when they occur under different reproductive conditions or life-history phases (C.X. Chan et al., unpublished). Here, we review Porphyra biology as a case study of how life history and stress tolerance research has led to the devel- opment of a lucrative, major crop; we also discuss why fields as diverse as evolutionary biology, aquaculture, physiological ecology, and comparative genomics and phy- logenomics will be impacted by the genome project. Development of a major crop of the sea The heteromorphic life history of Porphyra sensu lato consists of a gametophytic blade phase, which, after fertil- ization of the egg cell [14], produces zygotospores that grow into a shell-boring, branched, filamentous sporophyte called the conchocelis (originally described as a separate species, Conchocelis rosea). The conchocelis produces con- chospores that are released into the seawater and germi- nate to form new blades (Figure 1). The Porphyra blade is a Review Corresponding author: Brawley, S.H. (brawley@maine.edu). Glossary Allopolyploid: a species or cultivar whose cells have higher ploidy levels and chromosomes that are derived from two or more different species; allopoly- ploids are produced by some natural speciation events and by some artificial breeding experiments. Archeospores: asexual spores (n) formed by differentiation of a vegetative blade cell into a sporangium. The sporangium releases a single archeospore that germinates to form a new haploid blade. Previously referred to as monospores. Bangiales: the order to which Porphyra belongs (phylum Rhodophyta, class Bangiophyceae, order Bangiales, http://www.algaebase.org). Of the five currently recognized genera, Bangia, Dione and Minerva have filamentous gametophytes and sporophytes; Pseudobangia is filamentous but the full life history is unknown; Porphyra has a gametophytic blade (n) that alternates with a filamentous sporophyte (2n). Conchocelis: the filamentous sporophyte (2n) of species in the Bangiales. In nature, conchocelis occurs in calcareous matrices (e.g. mollusk shells) and releases conchospores at the surface of the matrix when mature. Meiosis occurs during germination of the conchospore to produce a new blade (n). Neutral spores: asexual spores (n) that are produced as a packet of spores within each sporangium on the blade of some Porphyra spp.; each haploid neutral spore germinates to form a new haploid blade. Phycobilisome: a structure that contains the photosynthetic accessory pigments phycoerythrin, phycocyanin and allophycocyanin. Phycobilisomes are attached to the thylakoid membrane in red algal chloroplasts. Pit plugs: a microscopic, glycoproteinaceous structure between the cells of the conchocelis in Bangiales. It is not found in the gametophyte (blade) phase. Zygotospores: ‘spores’ produced by successive cell divisions of the zygote. Zygotospores (2n) germinate to form the sporophyte phase (2n). TRPLSC-831; No. of Pages 9 1360-1385/$ – see front matter ß 2010 Published by Elsevier Ltd. doi:10.1016/j.tplants.2010.10.004 Trends in Plant Science xx (2010) 1–9 1