They can't move away from shade, so plants resort to a molecular solution to find a place in the sun. The action they take is quite radical, and involves a reprogramming of their development.
To survive, organisms must adapt to their ever-changing environment. Animals rely mainly on behavioural adaptive responses such as fighting or fleeing. But being stationary, plants must adjust their shape and metabolism accordingly. Plant hormones play an essential part in these adaptive responses, affecting various physiological and developmental processes. The hormone almost universally involved in plant adaptation is auxin. It exerts its effect at several developmental levels ranging from cell elongation and formation of the embryonic axis to fruit ripening1. Reporting in Cell, two teams — Tao et al.2 and Stepanova et al.3 — identify an enzyme that catalyses the first step in the biosynthesis of auxin, a step that occurs in response to changes in both ambient light and another plant hormone, ethylene.
A plant's repertoire of developmental tricks is extraordinarily broad: permanent stem-cell populations ensure growth throughout life; post-embryonic development allows new organs, such as leaves and flowers, to be generated; and differential growth enables developing plants to seek light, and roots to seek water. So even if plants have to compete — for example, for sunlight with their neighbours — they do so by modulating their own growth rather than by directly preventing that of others. Indeed, a reduction in the quality of light causes shade-avoidance syndrome, a physiological response leading to stem elongation, fewer branches and earlier flowering.
All of these processes are mediated by plant hormones, which, like animal hormones, do not necessarily act at the location at which they are synthesized. But unlike animals, plants lack a cardiovascular system, making effective distribution of hormones problematic. Consequently, the production of plant hormones is not as localized as that of their animal counterparts, and their effect typically depends on the activation of several hormonal pathways and crosstalk between them. Individual hormonal pathways in plants have been generally well characterized at a molecular level, but research into hormone crosstalk is still in its infancy.
For auxin, spatial differences in its concentration (forming auxin gradients) are crucial for specific developmental responses1. Local manipulation of cellular auxin levels — for example, by applying auxin in droplets or by locally activating its synthesis — confirmed4,5 that an increase in the level of this hormone triggers developmental programmes. So a central question in plant biology is how auxin gradients are generated. There are several answers. One is that specialized auxin-transport proteins mediate directional transport of the hormone. Asymmetric subcellular localization of these transporters ensures directional auxin movement between cells and can generate uneven auxin distribution6. Spatially restricted peaks in auxin levels can also be generated by local auxin biosynthesis7, although the biochemical pathways involved in this process are complex and remain poorly understood. Tao et al.2 and Stepanova et al.3 now identify an enzyme that is essential for local auxin biosynthesis and that markedly affects plant development.
Tao and colleagues performed a genetic screen to identify mutations in the plant Arabidopsis thaliana that compromise shade-avoidance responses. They detected the TAA1 gene, which when mutated prevents plant elongation under shady conditions. This mutant also has lower auxin levels and, in contrast to its normal counterpart, does not produce more auxin when placed in shade. Supplying external auxin restores the shade-avoidance response in taa1 mutants.
The authors' elaborate biochemical and structural analyses of TAA1 convincingly show that this enzyme catalyses conversion of the amino acid tryptophan to an auxin precursor, indole-3-pyruvic acid (Fig. 1). They also report that the expression of TAA1 is localized, being predominantly confined to the leaf margins, and that it increases under shady conditions. This finding is in line with the observed defects in shade-avoidance syndrome seen in taa1 mutants.
In addition to confirming the role of TAA1 in auxin biosynthesis, Stepanova and colleagues3 investigated the developmental relevance of this enzyme. They find two related genes that partially compensate for the loss of TAA1 function. But if all three genes are inactive, the consequences are disastrous: triple mutants are severely defective even during embryonic development, failing to generate a root. Only in certain combinations of the three mutations do plants survive, but at all developmental stages they still show strong, auxin-deficiency-related characteristics that are similar to the effect of mutations in YUCCA genes. (YUCCA genes encode enzymes that are also implicated in local auxin biosynthesis7.)
In a slight twist to the story, Stepanova et al. identify TAA1 in a screen for tissue-specific modulators of response to another essential plant hormone, ethylene. The taa1 mutants were insensitive to ethylene, but external auxin application restored their sensitivity, confirming earlier speculation8,9,10 about crosstalk between auxin and ethylene.
Taken together, these two papers2,3 unambiguously identify a central component of auxin biosynthesis and demonstrate its importance for specific developmental responses, as well as for hormone crosstalk. From a biochemical perspective, it will be interesting to see where, in relation to YUCCA, TAA1 resides in the auxin biosynthetic pathway, as the partially overlapping characteristics of these proteins' mutants indicate a common branch. Understanding the spatial and temporal regulation of TAA1, and expression of its related genes under different environmental conditions, is also of great interest for the exciting prospect of unravelling the mechanisms of signalling crosstalk in plants.
Tanaka, H. et al. Cell Mol. Life Sci. 63, 2738–2754 (2006).
Tao, Y. et al. Cell 133, 164–176 (2008).
Stepanova, A. N. et al. Cell 133, 177–191 (2008).
Reinhardt, D. et al. Nature 426, 255–260 (2003).
Dubrowski, J. et al. Proc. Natl Acad. Sci. USA (in the press).
Vieten, A. et al. Trends Plant Sci. 12, 160–168 (2007).
Cheng, Y. et al. Genes Dev. 20, 1790–1799 (2006).
Swarup, R. et al. Plant Cell 19, 2186–2196 (2007).
Stepanova, A. et al. Plant Cell 19, 2169–2185 (2007).
Ru˚z˘ic˘ka, K. et al. Plant Cell 19, 2197–2212 (2007).
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Distribution and change patterns of free IAA, ABP 1 and PM H+-ATPase during ovary and ovule development of Nicotiana tabacum L.
Journal of Plant Physiology (2012)
Journal of Theoretical Biology (2010)