Polar auxin transport: an early invention

Abstract

In higher plants, cell-to-cell polar auxin transport (PAT) of the phytohormone auxin, indole-3-acetic acid (IAA), generates maxima and minima that direct growth and development. Although IAA is present in all plant phyla, PAT has only been detected in land plants, the earliest being the Bryophytes. Charophyta, a group of freshwater green algae, are among the first multicellular algae with a land plant-like phenotype and are ancestors to land plants. IAA has been detected in members of Charophyta, but its developmental role and the occurrence of PAT are unknown. We show that naphthylphthalamic acid (NPA)-sensitive PAT occurs in internodal cells of Chara corallina. The relatively high velocity (at least 4–5 cm/h) of auxin transport through the giant (3–5 cm) Chara cells does not occur by simple diffusion and is not sensitive to a specific cytoplasmic streaming inhibitor. The results demonstrate that PAT evolved early in multicellular plant life. The giant Chara cells provide a unique new model system to study PAT, as Chara allows the combining of real-time measurements and mathematical modelling with molecular, developmental, cellular, and electrophysiological studies.

The number of cell types, information content, and the evolution of complex multicellularity

“…Curiously, a phylogenetic analysis using 360 plastid genes [20] identifies the Zygnematophyceae as the closest related group to the land plants. This relationship contrasts with the hypothesis that the charophycean algae, such as Chara and Coleochaete, are more closely related to the land plants (e.g., [15] features such as oogamy and plasmodesmata [21], and IAA polar transport [22]. The perplexing placement of the Zygnematophyceae in the streptophytes based on molecular data is explicable if considerable evolutionary reduction and loss of numerous synapomorphies (such as oogamy and flagellated sperm cells) occurred.…”

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…Directional transport of auxin in long, giant intermodal cells of Chara has been shown recently, suggesting that this phenomenon may be ancient (Boot et al 2012;Raven 2013). Some of the auxin biosynthetic enzymes entered the green lineage before the streptophyte-chlorophyte divergence, but the response and transport proteins characteristic of the well-studied auxin-signaling networks in angiosperms first appeared in charophytes, and the full complement of core auxin-signaling proteins became established in early embryophytes (Lau et al 2009;Prigge et al 2010;Wodniok et al 2011).…”

Diversity of phyllotaxis in land plants in reference to the shoot apical meristem structure

“…However, localization of PIN proteins in the plasma membranes in the seedless plants has to date only be confirmed in Physcomitrella [120]. Notably, PAT has also been identified in Chara (Characeae, green alga) [122], which shares a common ancestor with land plants, although PIN proteins in Chara are localized in the endoplasmic reticulum [123,124]. Although the auxin-regulated model of phyllotaxis formation is generally accepted for the seed plants, it does not explain all aspects of pattern formation; for instance, how the spatio-temporal polarization of PIN1 is regulated during organogenesis remains unknown, although several explanatory models have been proposed (e.g., [108,109,[125][126][127][128]).…”