JXB Advance Access published online on October 5, 2007
Journal of Experimental Botany, doi:10.1093/jxb/erm205
FOCUS PAPER |
The molecular analysis of the shade avoidance syndrome in the grasses has begun
Boyce Thompson Institute, Cornell University, Tower Road, Ithaca, NY 14853, USA
* To whom correspondence should be addressed. E-mail: tpb8{at}cornell.edu
Received 11 July 2007; Revised 8 August 2007 Accepted 13 August 2007
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Abstract |
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 Top Abstract IntroductionPhytochrome control of the...Light control of axillary...MAX genes regulate axillary...Role of auxin in...The regulation of flowering...Engineering plant architectureConclusionsReferences |
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The shade avoidance syndrome (SAS) is a morphological and physiological response initiated by a decrease in light quantity and a change in light quality. Recent work in Arabidopsis thaliana has begun to define the molecular components of the SAS in a model dicot species, but little is known of these networks in agronomically important grasses. The focus of this review is to present a current view of the SAS in the grasses based largely on the characterization of mutants in the phytochrome signal transduction pathway and on the effects of far-red light treatments on plant growth. In cereal grasses, intense selection by plant breeders has acted to attenuate some but not all shade avoidance responses within modern crop varieties. Traditionally, breeding efforts have been focused on optimizing grain yield. However, with the recent interest in lignocellulosic-based biofuels, a new breeding paradigm may emerge to optimize biomass at the expense of grain yield. Some of the opportunities and challenges for engineering plant architecture to maximize resource use efficiency and yield by targeting the SAS in grasses are discussed.
Key words: Biofuels, grasses, phytochrome, shade avoidance
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Introduction |
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TopAbstractIntroductionPhytochrome control of the...Light control of axillary...MAX genes regulate axillary...Role of auxin in...The regulation of flowering...Engineering plant architectureConclusionsReferences |
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Plants detect impending competition with neighbouring plants in part by measuring the relative proportion of red (R) light to far-red (FR) light in their environment (Ballare et al., 1990). Under full sunlight, plants are exposed to relatively equal fluxes of 600–700 nm (R) and 700–800 nm (FR) (Holmes and Smith, 1975, 1977). However, the majority of R light is absorbed, while FR light is largely reflected or transmitted to neighbouring vegetation (Cumming, 1963). Under persistent FR-rich light conditions, plants undergo a series of morphological changes that include reduced branching, increased plant height, and decreased leaf blade area (Smith, 1992, 1995). These morphological changes are accompanied by changes in physiology including a redistribution of auxin, enhanced ethylene production, and an acceleration of flowering (Smith, 1995; Finlayson et al., 1999; Morelli and Ruberti, 2000; Vandenbussche et al., 2003). Collectively, these traits have been termed the shade avoidance response or the shade avoidance syndrome (SAS) (Smith and Whitelam, 1997; Ballare, 1999).
In natural settings, a robust SAS allows plants to compete with neighbouring vegetation for limited resources (Dudley and Schmitt, 1996; Schmitt, 1997; Schmitt et al., 2003). However, this plasticity may come at a cost; recent studies using recombinant inbred lines of Arabidopsis suggest that plants with plastic responses for a number of traits (e.g. branching, senescence timing, and elongation) have lower fitness than fixed genotypes grown under high and low density (Weinig et al., 2006). Similarly, studies of Trifolium repens (white clover) suggest a fitness cost for a plastic petiole elongation response when plants are grown under high light conditions (Weijschede et al., 2006). For crop species, the SAS could lead to decreased yields if plants expend resources on vegetative growth at the expense of reproductive development. Thus, it is generally believed that shade avoidance responses have largely been attenuated during domestication (Smith, 1992). However, many cereal crops display a robust response to FR light signals (Casal et al., 1996; Maddonni et al., 2002; Morgan et al., 2002). These studies suggest that rather than simply attenuating the SAS, the SAS in crop plants has probably been refined to maximize yield under limited light environments (Maddonni et al., 2002). Given the strong selective pressure imposed by breeders who strive for increasing yields at increasing plant densities (Duvick, 1997), it is possible that some shade responses in crop plants may, in fact, be enhanced relative to their weedy relatives. The objective of this review is to highlight recent advances in our understanding of the molecular mechanisms underlying responses to vegetative shade, with a particular focus on the cereal crops.
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Phytochrome control of the SAS |
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TopAbstractIntroductionPhytochrome control of the...Light control of axillary...MAX genes regulate axillary...Role of auxin in...The regulation of flowering...Engineering plant architectureConclusionsReferences |
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In Arabidopsis, phytochrome B (phyB) and related photoreceptors phyD and phyE are believed to be the primary photoreceptors that perceive a change in R:FR light associated with vegetative shading (Halliday et al., 1994; Aukerman et al., 1997; Devlin et al., 1998, 1999; Franklin et al., 2003). This response is probably antagonized by the action of phyA (Mazzella et al., 1997; Cerdan et al., 1999) and the final manifestation of the response is likely to involve a complex interplay of photoreceptors, downstream signal transducers, and hormonal signalling networks (Vandenbussche et al., 2005).
To identify components of the SAS in Arabidopsis, gene expression profiling was conducted comparing plants grown in low and high R:FR light environments (Devlin et al., 2003; Salter et al., 2003; Roig-Villanova et al., 2006). These studies have identified both early- and late-acting genes that are induced or repressed in response to vegetative shade. Early-acting genes include the homeodomain leucine zipper transcriptional regulators ATHB-2 and ATHB-4, and the basic helix–loop–helix (bHLH) proteins PIL1 and HFR1 (Carabelli et al., 1996; Steindler et al., 1999; Salter et al., 2003; Sessa et al., 2005). Characterizations of two Arabidopsis transcription factors (ATHB-2 and PIL1) suggest that the SAS is initiated by transcriptional changes following a decrease in R:FR (Carabelli et al., 1996; Salter et al., 2003). These profiling studies also strengthened previous genetic studies which showed that phyA antagonizes phyB-mediated responses under prolonged low R:FR light conditions through the transcriptional control of target genes that include components of the auxin transport and signalling pathways (Devlin et al., 2003).
While ATHB-2 appears to function as a positive regulator of the SAS (Morelli and Ruberti, 2000), the roles of PIL1 and HFR1 are less clear (Sessa et al., 2005; Roig-Villanova et al., 2006). As HFR1 is a known component of phyA signal transduction (Fairchild et al., 2000; Fankhauser and Chory, 2000; Soh et al., 2000), it may enhance phyA-dependent antagonism of shade avoidance. Although pil1 mutants display an attenuated elongation response to transient low R:FR treatments (Salter et al., 2003), they also display a significant shift in the circadian phase of the response. Furthermore, PIL1 directly interacts with the clock component TOC1 (Makino et al., 2002). Thus, PIL1 may mediate responses to shade through interactions with the circadian clock. Characterization of shade-induced leaf movement (Mullen et al., 2006) further supports a role for the circadian control of at least some responses induced by shade.
In the grasses, the genetic dissection of light signal transduction networks is still in its infancy (Sawers et al., 2005). Unlike the higher eudicots, the phytochrome gene family in monocots contains only three members: PHYA, PHYB, and PHYC (Mathews and Sharrock, 1996, 1997). In maize (Zea mays), an allotetraploid event approximately 12 million years ago resulted in large segmental duplications within the present day maize genome (Gaut and Doebley, 1997). Analysis of the phytochrome gene family in maize has revealed duplications of all three gene family members in homeologous regions of the genome, suggesting that these duplications are a result of this allotetraploid event (Sheehan et al., 2004). phyB mutants have been identified in rice (Oryza sativa), maize, sorghum (Sorghum bicolor), and barley (Hordeum vulgare) (Childs et al., 1997; Hanumappa et al., 1999; Takano et al., 2005; Sheehan et al., 2007). phyB mutants of sorghum and phyB1 phyB2 double mutants of maize display many of the characteristics of a constitutive SAS, including increased plant height, increased internode length, reduced tillering, and early flowering (Pao and Morgan, 1986a, b; Childs et al., 1992, 1997; Sheehan et al., 2007). phyB1 mutants of sorghum display a rhythmic production of high ethylene levels with peaks that appear to be gated by the circadian clock (Finlayson et al., 1998). High levels of ethylene are also observed in wild-type sorghum plants grown under low R:FR, suggesting a role for ethylene in mediating the SAS (Finlayson et al., 1999). In rice, both phyB and phyC contribute to the repression of flowering time under non-permissive conditions (long days) (Takano et al., 2005). However, phyA phyB or phyA phyC double mutants flower significantly earlier than either the phyB or phyC single mutants, suggesting that in rice all three phytochrome genes contribute to flowering time variation. Given their roles in flowering time regulation, it is likely that phyA and phyC will also contribute to the SAS in the grasses.
To identify downstream components of the phytochrome signal transduction pathway in rice, Nakamura and colleagues recently examined the expression of several rice PIF/PIL homologues (Nakamura et al., 2007). There are approximately 170 bHLH proteins in rice and, although many share a high degree of homology with the bHLH domain of Arabidopsis homologues (Li et al., 2006), extensive genome rearrangements, duplication events, and gene loss between monocot and dicot lineages precludes the identification of orthologous relationships (Bennetzen, 2007). Thus, to define functional PIF/PIL homologues of rice, Nakamura et al. (2007) identified six genes from rice that contained the characteristic PIL and bHLH domains that define the Arabidopsis PIF gene family (Duek and Fankhauser, 2005) and ectopically expressed them in Arabidopsis seedlings. The majority of transgenic plants displayed elongated hypocotyls under light conditions that normally suppress hypocotyl elongation, suggesting that some of the rice PIF-like genes act to promote growth in a similar manner to some Arabidopsis PIF genes. These results should be interpreted with caution as a phenotype in Arabidopsis may reflect interactions with transcription factors that are either not present or not expressed in a similar temporal and spatial manner to the donor plant. Nevertheless, these findings are intriguing and suggest that a more detailed study of PIF/PIL function in the grasses is warranted.
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Light control of axillary meristem development |
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TopAbstractIntroductionPhytochrome control of the...Light control of axillary...MAX genes regulate axillary...Role of auxin in...The regulation of flowering...Engineering plant architectureConclusionsReferences |
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In the grasses, light quality and intensity have a profound effect on the developmental progression of vegetative meristem development (Doust, 2007). One of the most dramatic effects of shade in the grasses is on the production and proliferation of basal axillary meristems that develop into tillers (Casal et al., 1986, 1987a, b; Casal, 1988; Skinner and Simmons, 1993; Bahmani et al., 2000). In general, a reduction in R:FR results in increased apical dominance at the expense of tiller development.
Assessing the impact of reduced tiller number or development on yield is more complex. In maize, suppression of vegetative tillers has been targeted during domestication (Doebley et al., 1995, 1997, 2006). In sorghum, the grain yield and harvest index of tillering plants are lower than those of plants with a single culm under high planting density, presumably due to loss of resources used by the unproductive tillers (Lafarge et al., 2002). In barley, removal of vegetative tillers improves grain and straw yield (Elalaoui et al., 1988; Gu and Marshall, 1988). Conversely, high tillering varieties of rice are more productive than low tillering varieties under long growing seasons (Wu et al., 1998). Thus, in species or varieties in which tillering is a component of yield, it is likely that the tillering component of the SAS has been tempered to permit tiller production under high planting densities. In maize where tiller proliferation is often a negative component of yield, genetic variation may have been selected to enhance or maintain SAS-induced suppression of tillers.
In the monocot grasses, axillary meristems form in the axils of vegetative leaves or on the flanks of inflorescence meristems and give rise to tillers and flowers, respectively (McSteen and Leyser, 2005). Genes that control initiation of vegetative axillary meristems or outgrowth of vegetative buds (tillers) include Teosinte Branched1 (Tb1) and the rice orthologue fine culm1 (Doebley et al., 1997; Lukens and Doebley, 1999; Takeda et al., 2003), MONOCULM1 (Li et al., 2003), LAX PANICLE and SMALL PANICLE (Komatsu et al., 2003), Barren Stalk1 (Gallavotti et al., 2004), DWARF3 (Ishikawa et al., 2005), and HIGH TILLERING DWARF1 (Zou et al., 2005).
The most extensively characterized of these genes, Tb1, belongs to the TCP family of bHLH transcription factors (Cubas et al., 1999). Loss-of-function alleles of tb1 in maize result in a prolificacy of axillary branches, an architecture that resembles its wild ancestor teosinte (Zea mays ssp. parviglumis; Doebley et al., 1997). TCP proteins are classified as class I or class II and function as activators or repressors, respectively, of gene transcription by regulating the expression of growth- and cell cycle-related genes (Kosugi and Ohashi, 1997, 2002; Gaudin et al., 2000; Tremousaygue et al., 2003; Li et al., 2005). TB1, the product of the Tb1 gene, belongs to the class II family of TCP proteins and functions as a repressor of axillary bud outgrowth in maize and other monocots (Hubbard et al., 2002; Takeda et al., 2003). These studies and recent computational predictions have suggested that TCP proteins such as TB1 bind directly to cis-regulatory elements in the promoters of growth-regulating genes (Welchen and Gonzalez, 2006). However, direct targets of TB1 have yet to be defined in any plant species.
To explore the effects of vegetative shade on axillary shoot development in maize, Lukens and Doebley (1999) generated lines in which the ancestral teosinte allele of tb1 was introgressed into a standard maize inbred that produces few tillers. Maize plants homozygous for the introgressed teosinte allele of tb1 (Tb1-teosinte) were highly tillered under low density plantings. Interestingly, under canopy shade, the degree of tillering was greatly reduced. Furthermore, the decrease in tillering was directly related to increased expression of Tb1-teosinte. This result is consistent with the interpretation that TB1 acts to inhibit lateral shoot formation in maize (Doebley et al., 1997; Lukens and Doebley, 1999) and suggests that Tb1-teosinte is highly responsive to the light environment.
A more direct link between phytochrome and the regulation of axillary shoot development was recently revealed in studies of axillary branch development in sorghum (Kebrom et al., 2006). The ma3R allele of sorghum is a well characterized phyB mutant allele that conditions a constitutive shade avoidance response (Childs et al., 1997). Under low density plantings, tillering is inhibited in plants homozygous for the ma3R allele (also referred to as the phyB-1 mutant) during the vegetative stage of development, whereas the near-isogenic wild-type siblings branch prolifically (Fig. 1A). The inhibition of bud outgrowth is correlated with increased expression of the sorghum orthologue of the maize Tb1 gene (SbTB1), which is consistent with the function of TB1 in suppressing axillary bud outgrowth (Doebley et al., 1997; Hubbard et al., 2002; Takeda et al., 2003). These results led to the hypothesis that the control of dormancy and outgrowth of buds by light signals perceived by PHYB is linked to the regulation of expression of the SbTB1 in axillary buds (Kebrom et al., 2006). This study provides the first molecular evidence for a role for phytochrome in regulating branch meristem development and suggests an important role for phytochrome signalling in the regulation of this process (see Fig. 1B). Although most maize varieties do not produce tillers under typical planting densities, tillers are produced in many sweetcorn and popcorn varieties. Thus, to examine the role of PhyB1 in regulating tiller production in maize, a mutant phyB1 allele was recently introgressed into the sweetcorn inbred IL101. In preliminary screens, it appears that PhyB1 also promotes tiller development in maize (T Kebrom and T Brutnell, unpublished results).
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MAX genes regulate axillary branch development in grasses |
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TopAbstractIntroductionPhytochrome control of the...Light control of axillary...MAX genes regulate axillary...Role of auxin in...The regulation of flowering...Engineering plant architectureConclusionsReferences |
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Several mutants defective in bud outgrowth have recently been cloned and characterized including the ramosus (rms) mutants of pea (Pisum sativum) (Beveridge et al., 2000; Johnson et al., 2006), more axillary growth (max) mutants of Arabidopsis (Stirnberg et al., 2002; Sorefan et al., 2003; Booker et al., 2005), and decreased apical dominance (dad) mutants of petunia (Petunia hybrida) (Napoli, 1996; Snowden et al., 2005). These mutants are characterized by an increased number of vegetative branches. The identification of MAX1, MAX3, and MAX4 as biosynthetic enzymes involved in the generation of a carotenoid-derived product has defined a new class of signalling molecules necessary for suppressing bud outgrowth (Stirnberg et al., 2002; Sorefan et al., 2003; Booker et al., 2005). The MAX2 gene encodes an F-box protein that may be involved in the perception of the carotenoid-derived MAX signal (Stirnberg et al., 2002; Booker et al., 2005). The RMS and DAD genes of pea and petunia, respectively, are homologues to the Arabidopsis MAX genes (Sorefan et al., 2003; Snowden et al., 2005; Johnson et al., 2006). In rice, the branching mutants dwarf3 and high tillering dwarf1 are MAX2 and MAX3 orthologues, respectively (Ishikawa et al., 2005; Zou et al., 2005). Thus, there appear to be conserved mechanisms regulating bud dormancy and outgrowth among monocot and dicot lineages (Johnson et al., 2006).
However, differences in the regulation of the MAX genes are also apparent. In pea, MAX4/RMS1 expression is regulated by auxin, whereas the Arabidopsis MAX4 is not (Foo et al., 2005; Bainbridge et al., 2005). In addition, bud outgrowth is inhibited by application of auxin to a decapitated stem in pea but not in Arabidopsis (Cline, 1996). It is likely that additional variation will be observed in the monocot grasses as well given the strong positive and negative selection pressures that have been applied to various grass species through breeding programmes that aim to suppress (e.g. maize) or enhance (e.g. rice) tiller proliferation.
To identify additional genetic components of axillary branch development, Doust and colleagues conducted quantitative trait locus (QTL) analyses in foxtail millet (Setaria italica) and its wild relative green millet (Setaria viridis) (Doust et al., 2004, 2005). They detected several branching QTLs that were dependent on planting density but did not map to regions of the maize or rice genome with obvious gene candidates for regulating branching (e.g. Tb1 and PhyB1). These studies suggest that monocot grass species may have evolved multiple mechanisms to tolerate or respond to neighbouring vegetative shade. The use of QTL analysis may prove to be a particularly powerful approach to defining the SAS in maize, where populations have been developed to fine-map genetic variation (Stich et al., 2007).
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Role of auxin in mediating the SAS |
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TopAbstractIntroductionPhytochrome control of the...Light control of axillary...MAX genes regulate axillary...Role of auxin in...The regulation of flowering...Engineering plant architectureConclusionsReferences |
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Auxin has long been known to play a role in repressing axillary meristem development (McSteen and Leyser, 2005). Application of this plant hormone to a decapitated stump established that auxin synthesized in the shoot apex inhibits bud outgrowth (Thimann and Skoog, 1933; Cline, 1996). However, auxin does not directly enter the developing buds, suggesting that it mediates responses through second messengers (Stafstrom, 2000; Stafstrom et al., 1998; Leyser, 2005). Growing buds actively export auxin, facilitating the formation of vascular tissues that will connect the buds to the vascular system of the main stem through a process of canalization (Sachs, 1991). Recent molecular studies have indicated that the MAX signal regulates branching by controlling the transport of auxin (Bennett et al., 2006; Lazar and Goodman, 2006). The down-regulation of genes encoding auxin influx (AUX1) and efflux (PIN) carrier proteins in dormant buds of the wild type compared with the high levels of AUX1 and PIN expression in growing buds of max1 mutants is consistent with a role for auxin transport in mediating bud growth. Lazar and Goodman have suggested that MAX1 inhibits the export of auxin from the buds through the increased expression of genes involved in flavonoid biosynthesis which are known regulators of auxin transport (Brown et al., 2001; Lazar and Goodman, 2006). However, Leyser and colleagues contend that the MAX signal regulates the transport of auxin by controlling the expression of auxin transporter PIN genes and is independent of flavonoids (Bennett and Leyser, 2006).
Auxin has also been implicated in altering plant architecture in response to vegetative shade (Morelli and Ruberti, 2000, 2002). In maize, it appears that breeding programmes have targeted reduced auxin response in selecting for hybrids that grow well under high density plantings (Fellner et al., 2003). Thus, auxin may serve as an important transducer of light signals to regulate axillary branch development and other components of the SAS in the grasses.
Several studies have indicated that the target of endogenous signals, such as auxin, on bud dormancy and outgrowth is through the regulation of cell division (Stafstrom, 2000; Anderson et al., 2001). In Arabidopsis, overexpression of cyclin D2 reduces the duration of G1 phase and increases the growth rate (Cockcroft et al., 2000). In pea, the suspension of bud growth is associated with the down-regulation of several cell cycle-related genes (Devitt and Stafstrom, 1995; Shimizu and Mori, 1998), suggesting that the control of bud outgrowth is at least in part regulated through control of cell cycle progression. The repressed growth of dormant buds is also associated with increased expression of several dormancy-associated genes with unknown function, such as PsDRM1, PsDRM2, PsAD1, and PsAD2 (Stafstrom et al., 1998; Madoka and Mori, 2000). Although the downstream targets of phyB-regulated bud dormancy and outgrowth are unknown, recent studies in sorghum suggest that phytochromes may act independently of cell cycle-related genes to maintain cells in a dormant state (TH Kebrom, TP Brutnell, and SA Finlayson, unpublished results).
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The regulation of flowering time by light quality |
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TopAbstractIntroductionPhytochrome control of the...Light control of axillary...MAX genes regulate axillary...Role of auxin in...The regulation of flowering...Engineering plant architectureConclusionsReferences |
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Floral induction is a complex developmental process that integrates external inputs including temperature and photoperiod with autonomous and hormonal (gibberellin) signals (Blazquez and Weigel, 1999; Halliday et al., 2003; Balasubramanian et al., 2006; Corbesier and Coupland, 2006; Yan et al., 2006; Izawa, 2007). These multiple inputs ensure that flowering occurs under the appropriate environmental conditions. Several studies in monocot crops have associated lesions in the phytochrome signal transduction pathway with early flowering (Childs et al., 1997; Hanumappa et al., 1999; Izawa et al., 2000; Sawers et al., 2002; Takano et al., 2005; Sheehan et al., 2007). Taken together, these studies suggest that phytochromes play a universal role in regulating flowering in higher plants. However, as discussed above, while phyB appears to repress flowering in both monocots and dicots, the roles of phyA and phyC are less well conserved (Izawa, 2007).
One way in which phyB regulates flowering time appears to be through monitoring light quality. A lower R:FR ratio will indeed induce many plant species to flower precociously (Thomas, 2006). In Arabidopsis, this ‘light quality’ pathway is mediated by phyB and requires the nuclear-localized protein PHYTOCHROME AND FLOWERING TIME1 (PFT1). pft mutants are late flowering and completely suppress the early flowering phenotype of phyB in the phyB pft1 double mutant (Cerdan and Chory, 2003). Furthermore, pft mutants flower later than wild-type plants under conditions that simulate canopy shade. This delay in flowering is correlated with reduced accumulation of the floral activator FT (Samach et al., 2000), while expression of the transcription factor CONSTANS (Putterill et al., 1995) is relatively unaffected. These findings suggest that the light quality-sensing pathway acts independently of the photoperiod pathway and downstream of phyB to control the mobile flowering signal FT directly (Abe et al., 2005; Wigge et al., 2005; Corbesier et al., 2007; Tamaki et al., 2007). Interestingly, expression of phyB exclusively in leaf mesophyll cells is sufficient to rescue the early flowering defect of phyB under short day treatments and is correlated with reduced expression of FT (Endo et al., 2005). Whether or not the perception of light quality is mediated exclusively through leaf mesophyll cells remains to be seen.
Although several components of the flowering time network are conserved between monocots and dicots, there are significant points of divergence (Hayama and Coupland, 2004; Dubcovsky et al., 2006; Yan et al., 2006). In particular, no clear homologues of the flowering time repressor FLC (Michaels and Amasino, 1999) are present in rice, whereas no homologues of the rice flowering time regulator Ehd1 (Doi et al., 2004) are present in Arabidopsis (Izawa, 2007). In Arabidopsis, CO acts to promote flowering under long days, but the rice homologue Hd1 acts to delay flowering under long days (Hayama and Coupland, 2004). Furthermore, QTL studies in both rice and barley have identified variation at AP1 and FT as targets of selection, but screens of natural accessions of Arabidopsis have not yet revealed a link between allelic variation at AP1 and FT and floral invocation (Kojima et al., 2002; Gazzani et al., 2003; Yan et al., 2003, 2004, 2006; Balasubramanian et al., 2006; Corbesier et al., 2007; Tamaki et al., 2007). Thus, shade-induced flowering pathways may also have diverged significantly between monocot and dicot lineages.
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Engineering plant architecture |
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TopAbstractIntroductionPhytochrome control of the...Light control of axillary...MAX genes regulate axillary...Role of auxin in...The regulation of flowering...Engineering plant architectureConclusionsReferences |
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Traditionally, plant breeders have strived to optimize plant performance (yield) over a given area. Thus, yield per plant is not necessarily the ultimate objective in a breeding programme. In fact, per plant yields in maize have remained relatively constant over the past few decades, while yield per acre has continued to increase (Duvick, 1997). The genetic gains in yield can largely be attributed to breeding efforts that strive for consistent performance under high stress conditions (Duvick, 1997; Tollenaar and Wu, 1999), i.e. modern varieties show increased tolerance to heat, drought, low soil fertility, disease, and pest attack particularly under high density plantings (Troyer, 2001). As pressures on arable land continue to increase, it is likely that planting density will continue to be a target for selection in the years ahead.
One potential means of increasing performance of crop plants under high density plantings is to inhibit shade avoidance through the overexpression of phytochrome photoreceptors (Sawers et al., 2005). In potato (Solanum tuberosum), tomato (Solanum lycopersicum), rice, and tobacco (Nicotiana tabacum), overexpression of PHYA or PHYB generally results in shorter, bushier plants (Boylan and Quail, 1989; Keller et al., 1989; Nagatani et al., 1991; Robson et al., 1996; Halliday et al., 1997; Yanovsky et al., 1998; Thiele et al., 1999; Boccalandro et al., 2003; Garg et al., 2006). However, the morphological response to heterologous expression of PHY genes can vary dramatically even within a species. For instance, overexpression of the Arabidopsis PHYA gene in a Japonica variety of rice resulted in fewer tillers and a negative impact on yield, whereas expression of the same construct in an Indica variety correlated with increased tiller number and higher yield (Kong et al., 2004; Garg et al., 2006). Similarly, expression of rice or oat (Avena sativa) PHYA in the tobacco variety Xanthi reduced stem length and resulted in greener leaves, while expression of rice PHYA in variety SR1 did not result in any dramatic phenotypic effects (Kay et al., 1989; Keller et al., 1989; Nagatani et al., 1991). These studies suggest that the developmental plasticity of a given cultivar may vary considerably in response to the heterologous expression of phytochrome photoreceptors and highlight the inherent difficulties in extending the findings of model plant species to crop plants.
While the manipulation of the photoreceptors may provide a means to engineer whole plant responses, the consequences on yield are difficult to predict. Alternative strategies include the manipulation of downstream effectors of light signalling or to limit ectopic expression of transgenes to specific tissues or developmental phases of the plant. For instance, successful engineering of carotenoid composition in rice has been achieved through altering the expression of carotenoid biosynthetic enzymes using tissue-specific promoters (Paine et al., 2005). If increased tiller production is a target (e.g. rice or switchgrass), then it may be possible to reduce or enhance expression of a downstream component of the light response pathway using a promoter that is expressed only in axillary buds. An obvious advantage of this approach is that the risk of unforeseen morphological or physiological changes due to ectopic expression of the candidate transgene is greatly reduced. This is especially relevant when transcriptional regulators are manipulated, as many are capable of heterodimer formation and are usually under tight transcriptional control (Feller et al., 2006). An alternative strategy is to reduce the expression of a limited number of functionally redundant genes. For instance, a reduction in one of two cytochrome P450 genes involved in brassinosteroid biosynthesis results in rice plants with more upright leaves and a higher harvest index at high density plantings, whereas knocking out both genes resulted in severe dwarfing (Sakamoto et al., 2006). The high degree of gene duplication in the cereal genomes (Wei et al., 2007) suggests that selective inactivation of gene family members could be widely exploited as a general strategy to alter plant architecture subtly.
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Conclusions |
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TopAbstractIntroductionPhytochrome control of the...Light control of axillary...MAX genes regulate axillary...Role of auxin in...The regulation of flowering...Engineering plant architectureConclusionsReferences |
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With the advent of cost-effective and rapid sequencing technologies, we are rapidly expanding our knowledge of genes and their expression profiles in major food and biofuel crops including maize, sorghum, and switchgrass. One recent and exciting development is the drive to develop lignocellulosic-based biofuels. In the USA alone, nearly US$1 billion in industry (http://www.bp.com/sectiongenericarticle.do?categoryId=9017022&contentId=7030631) and government (http://genomicsgtl.energy.gov/centers/) support has been committed to this endeavour in the past year. One promising source of biofuels are perennial grasses such as switchgrass. These perennial species remobilize much of their nitrogen stores to the roots at the end of the yearly growing season, leaving behind carbon skeletons in the form of cellulose (Tilman et al., 2006). In these biofuel feedstocks, fermentability and biomass become the desired traits necessitating novel breeding strategies to achieve these goals. It is tempting to speculate that a detailed understanding of light response pathways in grasses will enable us to tailor these responses to meet the demands of plant breeding whether it be increased grain yield or increased biomass.
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Acknowledgements |
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The authors would like to acknowledge support from the Monsanto Company in preparing this review, and thank Patrice Dubois for discussions and critical comments on the manuscript.
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TopAbstractIntroductionPhytochrome control of the...Light control of axillary...MAX genes regulate axillary...Role of auxin in...The regulation of flowering...Engineering plant architectureConclusionsReferences |
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