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First published online 13 March 2008
doi: 10.1242/dev.016303

Development 135, 1503-1512 (2008)
Published by The Company of Biologists 2008
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Life-cycle-generation-specific developmental processes are modified in the immediate upright mutant of the brown alga Ectocarpus siliculosus

Akira F. Peters1,2,*, Delphine Scornet1,2, Morgane Ratin1,2, Bénédicte Charrier1,2, Annabelle Monnier3, Yves Merrien1,2, Erwan Corre4, Susana M. Coelho1,2 and J. Mark Cock1,2,{dagger}

1 UPMC Université Paris 06, The Marine Plants and Biomolecules Laboratory, UMR 7139, Station Biologique de Roscoff, Place Georges Teissier, BP74, 29682 Roscoff Cedex, France.
2 CNRS, UMR 7139, Laboratoire International Associé Dispersal and Adaptation in Marine Species, Station Biologique de Roscoff, Place Georges Teissier, BP74, 29682 Roscoff Cedex, France.
3 Microarray Platform, OUEST-Génopole, Université de Rennes 1-Faculté de Médecine, Campus de Villejean, 35043 RENNES Cédex, France.
4 Computer and Genomics resource Centre, FR 2424, Station Biologique de Roscoff, Place Georges Teissier, BP74, 29682 Roscoff Cedex, France.


Figure 1
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  		Fig. 1. Life history of Ectocarpus in culture. The sexual cycle (left) involves an alternation between the diploid sporophyte and haploid dioecious (male and female) gametophytes. The sporophyte produces meio-spores, via a meiotic division (R!), in the unilocular (single-chambered) sporangia. The meio-spores are released and develop as gametophytes, which produce gametes in plurilocular gametangia. Fusion of male and female gametes produces a zygote (F!). The zygote develops as a diploid sporophyte, completing the sexual cycle. Unfertilised gametes can enter a parthenogenetic asexual cycle by germinating without fusion to produce a partheno-sporophyte (right). The partheno-sporophyte produces spores in unilocular sporangia and these develop as gametophytes, completing the parthenogenetic, asexual cycle. The parthenogenetic, asexual pathway is shown only for a male, but female gametes can also develop parthenogenetically. Two additional pathways of asexual reproduction are possible. The first involves the production, by sporophytes, of mito-spores in plurilocular sporangia. These spores reproduce the sporophyte stage (dashed lines). In addition, a proportion of the meio-spores may develop as sporophytes rather than gametophytes (dotted line). This latter phenomenon is also observed with the partheno-sporophyte but this has been omitted to simplify the diagram. R!, meiotic reduction; F!, gamete fusion.

 

Figure 2
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  		Fig. 2. Development of the Ectocarpus gametophyte. (A) Two germinating meiospores, the uppermost showing initiation of the second germ tube (arrowhead). (B) Germinating meiospore after 4 days growth, with a rhizoid developed from the first (lower) germ tube and an upright filament from the second (upper) germ tube. (C) Five-day-old germinating meiospore in which only the rhizoid has developed so far. (D) Gametophyte 1 week after germination; upright filament still unbranched. The cell corresponding originally to the meiospore is indicated by an arrow in A-D. (E) Branching of the upright filament. (F) Mature, richly branched gametophyte; arrow indicates the base of the thallus. (G) Gametangium. (H) Beginning of the formation of additional rhizoids from basal ends of cells of the upright filament. (I) Rhizoids covering an older upright filament. Scale bars: in F, 200 µm; in all other micrographs, 20 µm.

 

Figure 3
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  		Fig. 3. Development of the Ectocarpus sporophyte. (A) Zygote, the two eyespots are visible (arrows). (B,C) Development of the first germ tube. (D) Initiation of the second germ tube. (E) Prostrate filament after 2 weeks, older cells (including the original zygote cell) round up. (F) Branching of the prostrate filament. (G) Upright filament developed from a prostrate base. (H) Transition between prostrate base and upright filament of the thallus shown in G. Note the `string of pearls' shape of the cells of the prostrate filament, contrasting with the regular cylindrical shape of the cells of the upright filament; arrows indicate a rhizoid formed near the base of the upright filament. (I) Mature, six-week-old sporophyte with a well-developed prostrate basal system (arrow) and upright filaments emerging from it. (J) Plurilocular sporangium (mitosporangium). (K) Unilocular sporangium (meiosporangium). zc, original zygote cell. Scale bars: 5 µm in A-D; 20 µm in E,H; 40 µm in F,G,J,K; 100 µm in I. A-D are reproduced, with permission, from Peters et al. (Peters et al., 2004bGo).

 

Figure 4
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  		Fig. 4. Photopolarisation of mutant and wild-type Ectocarpus germlings in response to unidirectional light. Error bars show standard deviations. The negative phototropic response of the wild-type gametophyte was significantly more marked that those of the wild-type and imm sporophytes ({chi}2=25.68, P<0.001). wt SP A, wild-type partheno-sporophytes; wt SP B, wild-type sporophytes from mito-spores; wt GA, wild-type gametophytes; imm SP, imm partheno-sporophytes, n, number of individuals scored in each population.

 

Figure 5
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  		Fig. 5. Development of the imm mutant sporophyte. (A) First germ tube of germinating zygote cell homozygous for imm. (B) Germling at a later stage, with a rhizoid developed from the first germ tube (below) and an upright filament from the second germ tube (above). The cell corresponding to the original zygote is indicated by an arrow. (C) Mature, six-week-old imm mutant sporophyte with well developed, richly branched upright filaments. The arrow indicates the point of attachment to the substratum. (D,E) Macroscopic views of five-week-old thalli of imm and wild-type sporophytes, respectively, illustrating the marked difference in morphology. The wild type has formed a dense prostrate basal system. The imm mutant lacks this structure; it possesses a well-developed, but diffuse, erect thallus which is not as easily visualised with the naked eye. (F) Plurilocular sporangium on an imm mutant sporophyte. (G) Unilocular sporangium on an imm mutant sporophyte. Scale bars: 10 µm in A,B; 250 µm in C; 1 cm in D,E; 20 µm in F,G.

 

Figure 6
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  		Fig. 6. Summary of the crosses carried out for the genetic analysis of the imm mutation. Refer to Table 2 for the strain codes (e.g. Ec 17). The genotype is shown in brackets. SP, sporophyte, GA, gametophyte.

 

Figure 7
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  		Fig. 7. Microarray analysis of the expression of genes corresponding to two subtraction libraries enriched for sporophyte- and gametophyte-specific cDNAs in wild-type and imm partheno-sporophytes. Relative abundance of transcripts corresponding to genes identified by suppression subtraction hybridisation in (A) two independent wild-type partheno-sporophyte samples and (B) a wild-type partheno-sporophyte and an imm mutant partheno-sporophyte sample. Sequences corresponding to the sporophyte SSH library are shown in pink, sequences corresponding to the gametophyte SSH library are shown in blue. (C) The same graph as shown in B except that genes that are significantly upregulated in the imm mutant partheno-sporophyte compared with the wild type are highlighted in yellow and genes that are significantly downregulated in light blue. wt SP A and wt SP B, two independent wild-type partheno-sporophyte cDNA targets; imm SP, imm mutant partheno-sporophyte cDNA target.

 

Figure 8
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  		Fig. 8. Quantitative PCR analysis of the abundances of gene transcripts in young partheno-sporophytes and gametophytes of both the wild type and the imm mutant strain. The genes assayed are described in more detail in Table 3. Error bars show standard deviations. wt SP, wild-type partheno-sporophyte; wt GA, wild-type gametophyte; imm SP, imm partheno-sporophyte; imm GA, imm gametophyte.

 

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