Auxin Metabolism and Function in the Multicellular Brown AlgaEctocarpus siliculosus   

Abstract

Ectocarpus siliculosus is a small brown alga that has recently been developed as a genetic model. Its thallus is filamentous, initially organized as a main primary filament composed of elongated cells and round cells, from which branches differentiate. Modeling of its early development suggests the involvement of very local positional information mediated by cell-cell recognition. However, this model also indicates that an additional mechanism is required to ensure proper organization of the branching pattern. In this paper, we show that auxin indole-3-acetic acid (IAA) is detectable in mature E. siliculosus organisms and that it is present mainly at the apices of the filaments in the early stages of development. An in silico survey of auxin biosynthesis, conjugation, response, and transport genes showed that mainly IAA biosynthesis genes from land plants have homologs in the E. siliculosus genome. In addition, application of exogenous auxins and 2,3,5-triiodobenzoic acid had different effects depending on the developmental stage of the organism, and we propose a model in which auxin is involved in the negative control of progression in the developmental program. Furthermore, we identified an auxin-inducible gene called EsGRP1 from a small-scale microarray experiment and showed that its expression in a series of morphogenetic mutants was positively correlated with both their elongated-to-round cell ratio and their progression in the developmental program. Altogether, these data suggest that IAA is used by the brown alga Ectocarpus to relay cell-cell positional information and induces a signaling pathway different from that known in land plants.

Evolution of growth-promoting plant hormones

“…The recent identification of auxin and its proposed actions in a brown algal model, Ectocarpus siliculosus (Le Bail et al 2010), may lend support to the latter hypothesis. However, this raises the question of how the systems were recruited in different phylogenetic groups (e.g.…”

“…Lau et al (2009) reviewed the evidence that auxin can have physiological effects on algal growth, as well as evidence to the contrary, and concluded by doubting the functional relevance of auxin in algae, suggesting instead that IAA may simply be a byproduct of tryptophan. However, a recent paper on the brown alga E. siliculosus suggests a role for IAA in development, although the response pathway appears to be different to that in vascular plants ( Le Bail et al 2010).…”

“…Consistent with that, Rensing et al (2008) reported that genes thought to be related to auxin homeostasis were not found in the genomes of the aquatic unicellular green algae Ostreococcus tauri, Ostreococcus lucimarinus and Chlamydomonas reinhardtii. However, IAA has been identified in multicellular algae, including Fucus distichus and Ectocarpus siliculosus (Basu et al 2002;Le Bail et al 2010), and importantly, Nitella spp. (Sztein et al 2000).…”

Seaweed reproductive biology: environmental and genetic controls

“…The best explored putative phytohormones in brown algae are auxins, which exert a growth-promoting function in land plants, but most research has concentrated on the effects of indole-3-acetic (IAA) on growth and cell polarity, rather than its influence on fertility (Basu et al 2002, Lin and Stekoll 2007, Le Bail et al 2010. Auxin was shown to promote growth and inhibit sporogenesis when applied exogenously to Saccharina japonica, and the auxin oxidase activity in sporophyllous tissue was shown to be dramatically increased (Kai et al 2006).…”

Dynamical patterning modules in plant development and evolution

“…It is likely that elements of this module were present in unicellular plants since the cell walls of unicellular algae are not mechanically isotropic and manifest morphologies that are distinctly non-spherical. In addition, endogenous auxin has been identified in some multicellular algae (Boot et al, 2012), even in lineages that are not related to the green algal and land plant clade (e.g., the brown alga Ectocarpus siliculosus, in which auxin might play a crucial role in the elongation of the filamentous thallus; Le Bail et al, 2010). Likewise, the effects of auxins on the dynamics of the cytoskeleton of unicellular charophycean algae appear to be similar to those observed for embryophytes (Jin et al, 2008).…”