Santa Clara University Scholar Commons Biology College of Arts & Sciences 4-2009 Plant Defense: a Pre-adaptation for Pollinator Shifts Justen B. Whittall Santa Clara University, [email protected] Matthew L. Carlson Follow this and additional works at: http://scholarcommons.scu.edu/bio Part of the Ecology and Evolutionary Biology Commons, and the Plant Sciences Commons Recommended Citation New Phytologist. Volume 182, Issue 1, April 2009, Pages: 5-8. Justen Whittall and Matthew Carlson. This Article is brought to you for free and open access by the College of Arts & Sciences at Scholar Commons. It has been accepted for inclusion in Biology by an authorized administrator of Scholar Commons. For more information, please contact [email protected]. Forum CommentaryBlackwellOxford,NPHNew1469-8137©277110.1111/j.1469-8137.2009.02771.xJanuary0??? The Phytologist Authors UK2009 Publishing (2009). Ltd Journal compilation © New Phytologist (2009) Commentary Cominelli et al., 2007; Lea et al., 2007). While much is known Pigment loss in response to about how anthocyanin production is positively regulated the environment: a new role in response to various conditions, little is known about the mechanisms responsible for anthocyanin catabolism in response for the WD/bHLH/MYB to certain environmental stimuli. In this issue of New Phytologist, Rowan and colleagues (pp. 102–115) provide new insights anthocyanin regulatory that enhance our understanding of anthocyanin pathway regulation by the TTG1/bHLH/MYB complex in response to complex conditions that promote anthocyanin turnover and degradation. This work is unique in its approach; not only examining anthocyanin turnover and degradation in Arabidopsis as a response The bright reds, blues and purples produced in most plants by to environmental conditions promoting pigment loss, but also the anthocyanin biosynthetic pathway have been of perennial establishing a novel connection to the Arabidopsis TTG1/bHLH/ fascination to plant biologists. Being conspicuously colorful, MYB complex. This is in refreshing contrast to numerous dispensable and tractable have made these flavonoid-based studies over the years emphasizing primarily the production pigments ideal subjects for studying a variety of biological of pigments through the positive regulation of anthocyanin phenomena in a number of plant models. Indeed, seed coat and biosynthesis by the TTG1-dependent transcriptional complex. flower color of peas were among the phenotypes used by Gregor Mendel in his studies of inheritance, and Barbara McClintock followed curious color changes in maize kernels in her discovery of transposable elements. More recently, in petunia, anthocyanin loss as a result of the overexpression of flavonoid biosynthetic ‘The work of Rowan et al. defines a new role for the genes, first noticed by Richard Jorgensen and colleagues, helped to define the phenomenon of cosuppression (RNA interference WD/bHLH/MYB anthocyanin regulatory complex by or RNA mediated gene silencing) (Napoli et al., 1990; Jorgensen, showing that it mediates the response to environmental 1995). A significant part of this rich research tradition is a wealth of work on transcriptional regulation in plants for stimuli which promote pigment loss.’ which the anthocyanin pathway has been an excellent model. In fact, the first plant transcription factor cloned was Colorless1 (C1) (Cone et al., 1986), a maize MYB regulator of the flavonoid pigment biosynthetic pathway. From this, and from subsequent work in a host of plant species, emerged the now canonical WD-repeat/bHLH/MYB combinatorial transcription New twists on old favorites factor complex model for the regulation of the anthocyanin pathway (Goff et al., 1992; Spelt et al., 2000; Zhang et al., The PAP1 MYB regulator of the anthocyanin pathway was 2003; Schwinn et al., 2006; Gonzalez et al., 2008). The story first identified in striking fashion by an activation tag screen; in Arabidopsis is particularly interesting as there are four R2R3 the Arabidopsis mutant overexpressing this MYB appears to be MYB activators (PAP1, PAP2, MYB113 and MYB114), three deeply pigmented over much of the plant body and life cycle bHLH activators (TT8, EGL3 and GL3) and at least one R3 (Borevitz et al., 2000). This was apparently a result of the repressor (MYBL2) that can physically interact with each other upregulation of not just a subset of anthocyanin structural genes, to form various transcriptional complexes with the WD-repeat but genes across the entire general phenylpropanoid pathway protein, TTG1 (Gonzalez et al., 2008; Matsui et al., 2008). This (Borevitz et al., 2000; Tohge et al, 2005). Seemingly broad suggests a combinatorial transcription factor mechanism regulation of phenylpropanoid metabolism, coupled with a behind the fine regulation of pigment expression observed dramatic gain-of-function phenotype, made the PAP1 over- developmentally and in response to various biotic and abiotic expressor mutant a fascinating research subject with possibly stresses. Indeed, we have begun to elucidate the molecular much to tell about transcriptional control invested in a single mechanisms of how the Arabidopsis regulators differentially transcription factor over a considerable swath of metabolic contribute to pigment production in response to specific pathway. While the subsequent emphasis on what PAP1 can stimuli that promote pigment production (Teng et al., 2005; do when overexpressed proved fruitful in identifying new © The Author (2009). New Phytologist (2009) 182: 1–3 1 Journal compilation © New Phytologist (2009) www.newphytologist.org 1 2 Forum Commentary anthocyanin pathway genes (Tohge et al., 2005), questions that it mediates the response to environmental stimuli which lingered about the limitations of this MYB, about native pathway promote pigment loss. By altering the composition of the regulation by PAP1 and about the contributions to anthocyanin transcriptional complex in response to HTLL, regulation of pathway regulation by the closely related paralogous MYBs, anthocyanin pathway genes is achieved. However, the questions namely PAP2, MYB113 and MYB114. Some of these questions remain of what links the expression changes of regulatory have only recently been addressed, again with the help of PAP1 genes, such as TT8 and EGL3, to the environment; and what overexpressor mutants (Teng et al., 2005; Cominelli et al., connects the WD/bHLH/MYB complex particularly to 2007; Lea et al., 2007; Gonzalez et al., 2008). abiotic conditions that cause anthocyanin loss? Despite a However, the work of Rowan and colleagues presents a clever research history of MYB and bHLH anthocyanin regulators twist on the use of the PAP1 overexpressor. These authors spanning two decades, virtually nothing is known about what identify an environmental condition (high temperature, low directly influences members of this heavily studied complex in light; HTLL) that results in the reversible loss of pigmentation response to biotic and abiotic stimuli. Hormones have been despite the overexpression of PAP1. In-depth profiling of antho- implicated in influencing the expression or function of the cyanin content and biosynthetic gene expression indicates that complex but, again, it is not known how many steps removed pigment loss caused by HTLL is a function of both anthocy- this regulation might be from direct control of the regulators. anin turnover and downregulation of the flavonoid pathway, Research efforts that move upstream of the WD/bHLH/MYB consistent with previous work in grape and rose (Dela et al., complex are warranted and should reveal new mechanisms that 2003; Mori et al., 2007). But, unlike previous studies, new help translate environmental stimuli to control of the flavonoid mechanisms are proposed that account for the downregulation biosynthetic pathway. of the anthocyanin pathway and loss of pigments in plants under HTLL. First, other members of the anthocyanin-regulatory Antonio Gonzalez complex, such as EGL3 and TT8 bHLH genes, and TTG1 encoding the WD-repeat protein, are downregulated by HTLL The University of Texas at Austin, 2500 Speedway, treatment. Second, the gene encoding the R3 repressor MYB Austin TX 78712, USA (MYBL2), which competes with R2R3 activator MYBs for (tel +1 512 471 3553; email [email protected]) binding to bHLH partners, is upregulated by HTLL treatment. This, in turn, would explain decreases in the expression of anthocyanin structural genes, even when PAP1 is overexpressed. References This is an important finding with respect to the long-studied Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C. 2000. Activation tagging WD-repeat/bHLH/MYB anthocyanin regulatory complex; it identifies a conserved MYB regulator of phenylpropanoid biosynthesis. demonstrates that the complex itself is robustly targeted (by the Plant Cell 12: 2383–2394. Cominelli E, Gusmaroli G, Allegra D, Galbiati M, Wade HK, Jenkins GI, downregulation of activator members and by the upregulation Tonelli C. 2007. Expression analysis of anthocyanin regulatory genes in of repressor members) as a novel mechanism mediating the response to different light qualities in Arabidopsis thaliana. Journal of Plant response of anthocyanin loss to abiotic conditions. Physiology 165: 886–894. Another interesting mechanism possibly contributing to the Cone KC, Burr FA, Benjamin B. 1986. Molecular analysis of the maize loss of anthocyanins under HTLL treatment is suggested by the anthocyanin regulatory locus c1. Proceedings of the National Academy of Sciences, USA