Light intensity modulates the regulatory network of the shade avoidance response in Arabidopsis.
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ABSTRACT:
SUBMITTER: Hersch M
PROVIDER: S-EPMC4035961 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Quantitative Trait Loci (QTL) analyses in immortal populations are a powerful method for exploring the genetic mechanisms that control interactions of organisms with their environment. However, QTL analyses frequently do not culminate in the identification of a causal gene due to the large chromosomal regions often underlying QTLs. A reasonable approach to inform the process of causal gene identification is to incorporate additional genome-wide information, which is becoming increasingly accessible. In this work, we perform QTL analysis of the shade avoidance response in the Bayreuth-0 (Bay-0, CS954) x Shahdara (Sha, CS929) recombinant inbred line population of Arabidopsis. We take advantage of the complex pleiotropic nature of this trait to perform network analysis using co-expression, eQTL and functional classification from publicly available datasets to help us find good candidate genes for our strongest QTL, SAR2. This novel network analysis detected EARLY FLOWERING 3 (ELF3; AT2G25930) as the most likely candidate gene affecting the shade avoidance response in our population. Further genetic and transgenic experiments confirmed ELF3 as the causative gene for SAR2. The Bay-0 and Sha alleles of ELF3 differentially regulate developmental time and circadian clock period length in Arabidopsis, and the extent of this regulation is dependent on the light environment. This is the first time that ELF3 has been implicated in the shade avoidance response and that different natural alleles of this gene are shown to have phenotypic effects. In summary, we show that development of networks to inform candidate gene identification for QTLs is a promising technique that can significantly accelerate the process of QTL cloning.
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Project description:BackgroundOptimization of shade avoidance response (SAR) is crucial for enhancing crop yield in high-density planting conditions in modern agriculture, but a comprehensive study of the regulatory network of SAR is still lacking in monocot crops.ResultsIn this study, the genome-wide early responses in maize seedlings to the simulated shade (low red/far-red ratio) and also to far-red light treatment were transcriptionally profiled. The two processes were predominantly mediated by phytochrome B and phytochrome A, respectively. Clustering of differentially transcribed genes (DTGs) along with functional enrichment analysis identified important biological processes regulated in response to both treatments. Co-expression network analysis identified two transcription factor modules as potentially pivotal regulators of SAR and de-etiolation, respectively. A comprehensive cross-species comparison of orthologous DTG pairs between maize and Arabidopsis in SAR was also conducted, with emphasis on regulatory circuits controlling accelerated flowering and elongated growth, two physiological hallmarks of SAR. Moreover, it was found that the genome-wide distribution of DTGs in SAR and de-etiolation both biased toward the maize1 subgenome, and this was associated with differential retention of various cis-elements between the two subgenomes.ConclusionsThe results provide the first transcriptional picture for the early dynamics of maize phytochrome signaling. Candidate genes with regulatory functions involved in maize shade avoidance response have been identified, offering a starting point for further functional genomics investigation of maize adaptation to heavily shaded field conditions.
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Project description:Branching is an important trait of plant development regulated by environmental signals. Phytochromes in Arabidopsis mediate branching in response to the changes in the red light:far-red light ratio (R:FR), the mechanisms of which are still elusive. Here it is shown that overexpression of CONSTANS-LIKE 7 (COL7) results in an abundant branching phenotype which could be efficiently suppressed by shade or a simulated shade environment (low R:FR). Moreover, col7 mutants develop shorter hypocotyls and COL7 overexpression lines develop longer hypocotyls in comparison with the wild type in low R:FR, indicating that COL7 acts as an enhancer of the shade avoidance response. In shade or transient low R:FR, transcriptional and post-transcriptional expression levels of COL7 are up-regulated and positively associated with rapid mRNA accumulation of PHYTOCHROME INTERACTING FACTOR 3-LIKE 1 (PIL1), a marker gene of shade avoidance syndrome (SAS). Taken together, the results suggest a dual role for COL7 which promotes branching in high R:FR conditions but enhances SAS in low R:FR conditions.
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Project description:Plants have evolved strategies to avoid shade and optimize the capture of sunlight. While some species are tolerant to shade, plants such as Arabidopsis thaliana are shade-intolerant and induce elongation of their hypocotyl to outcompete neighboring plants. We report the identification of a developmental module acting downstream of shade perception controlling vascular patterning. We show that Arabidopsis plants react to shade by increasing the number and types of water-conducting tracheary elements in the vascular cylinder to maintain vascular density constant. Mutations in genes affecting vascular patterning impair the production of additional xylem and also show defects in the shade-induced hypocotyl elongation response. Comparative analysis of the shade-induced transcriptomes revealed differences between wild type and vascular patterning mutants and it appears that the latter mutants fail to induce sets of genes encoding biosynthetic and cell wall modifying enzymes. Our results thus set the stage for a deeper understanding of how growth and patterning are coordinated in a dynamic environment.
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Project description:After nitrogen treatments, plant leaves become narrower and thicker, and the chlorophyll content increases. However, the molecular mechanisms behind these regulations remain unknown. Here, we found that the changes in leaf width and thickness were largely compromised in the shade avoidance 3 (sav3) mutant. The SAV3 gene encodes an amino-transferase in the auxin biosynthesis pathway. Thus, the crosstalk between shade and nitrogen in Arabidopsis leaf development was investigated. Both hypocotyl elongation and leaf expansion promoted by the shade treatment were reduced by the high-N treatment; high-N-induced leaf narrowing and thickening were reduced by the shade treatment; and all of these developmental changes were largely compromised in the sav3 mutant. Shade treatment promoted SAV3 expression, while high-N treatment repressed SAV3 expression, which then increased or decreased auxin accumulation in cotyledons/leaves, respectively. SAV3 also regulates chlorophyll accumulation and nitrogen assimilation and thus may function as a master switch responsive to multiple environmental stimuli.
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Project description:Shade avoidance is an ecologically and molecularly well-understood set of plant developmental responses that occur when the ratio of red to far-red light (R:FR) is reduced as a result of foliar shade. Here, a genome-wide association study (GWAS) in Arabidopsis thaliana was used to identify variants underlying one of these responses: increased hypocotyl elongation. Four hypocotyl phenotypes were included in the study, including height in high R:FR conditions (simulated sun), height in low R:FR conditions (simulated shade), and two different indices of the response of height to low R:FR. GWAS results showed that variation in these traits is controlled by many loci of small to moderate effect. A known PHYC variant contributing to hypocotyl height variation was identified and lists of significantly associated genes were enriched in a priori candidates, suggesting that this GWAS was capable of generating meaningful results. Using metadata such as expression data, GO terms, and other annotation, we were also able to identify variants in candidate de novo genes. Patterns of significance among our four phenotypes allowed us to categorize associations into three groups: those that affected hypocotyl height without influencing shade avoidance, those that affected shade avoidance in a height-dependent fashion, and those that exerted specific control over shade avoidance. This grouping allowed for the development of explicit hypotheses about the genetics underlying shade avoidance variation. Additionally, the response to shade did not exhibit any marked geographic distribution, suggesting that variation in low R:FR-induced hypocotyl elongation may represent a response to local conditions.
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Project description:Plants that grow in high density communities activate shade avoidance responses to consolidate light capture by individuals. Although this is an evolutionary successful strategy, it may not enhance performance of the community as a whole. Resources are invested in shade responses at the expense of other organs and light penetration through the canopy is increased, allowing invading competitors to grow better. Here we investigate if suppression of shade avoidance responses would enhance group performance of a monoculture community that is invaded by a competitor. Using different Arabidopsis genotypes, we show that suppression of shade-induced upward leaf movement in the pif7 mutant increases the pif7 communal performance against invaders as compared to a wild-type canopy. The invaders were more severely suppressed and the community grew larger as compared to wild type. Using computational modelling, we show that leaf angle variations indeed strongly affect light penetration and growth of competitors that invade the canopy. Our data thus show that modifying specific shade avoidance aspects can improve plant community performance. These insights may help to suppress weeds in crop stands.
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Project description:Plants that are adapted to environments where light is abundant are especially sensitive to competition for light from neighboring vegetation. As a result, these plants initiate a series of changes known as the shade avoidance syndrome, during which plants elongate their stems and petioles at the expense of leaf development. Although the developmental outcomes of exposure to prolonged shade are known, the signaling dynamics during the initial exposure of seedlings to shade is less well studied. Here, we report the development of a new software-based tool, called HyDE (Hypocotyl Determining Engine) to measure hypocotyl lengths of time-resolved image stacks of Arabidopsis wild-type and mutant seedlings. We show that Arabidopsis grows rapidly in response to the shade stimulus, with measurable growth after just 45 min shade exposure. Similar to other mustard species, this growth response occurs in multiple distinct phases, including two phases of rapid growth and one phase of slower growth. Using mutants affected in shade avoidance phenotypes, we demonstrate that most of this early growth requires new auxin biosynthesis via the indole-3-pyruvate pathway. When activity of this pathway is reduced, the first phase of elongation growth is absent, and this is correlated with reduced activity of auxin-regulated genes. Finally, we show that varying shade intensity and duration can affect the shape and magnitude of the growth response, indicating a broad range of the elongation response to shade.
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Project description:Sun-loving plants perceive the proximity of potential light-competing neighboring plants as a reduction in the red:far-red ratio (R:FR), which elicits a suite of responses called the "shade avoidance syndrome" (SAS). Changes in R:FR are primarily perceived by phytochrome B (phyB), whereas UV-B perceived by UV RESISTANCE LOCUS 8 (UVR8) elicits opposing responses to provide a counterbalance to SAS, including reduced shade-induced hypocotyl and petiole elongation. Here we show at the genome-wide level that UVR8 broadly suppresses shade-induced gene expression. A subset of this gene regulation is dependent on the UVR8-stabilized atypical bHLH transcription regulator LONG HYPOCOTYL IN FAR-RED 1 (HFR1), which functions in part redundantly with PHYTOCHROME INTERACTING FACTOR 3-LIKE 1 (PIL1). In parallel, UVR8 signaling decreases protein levels of the key positive regulators of SAS, namely the bHLH transcription factors PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and PIF5, in a COP1-dependent but HFR1-independent manner. We propose that UV-B antagonizes SAS via two mechanisms: degradation of PIF4 and PIF5, and HFR1- and PIL1-mediated inhibition of PIF4 and PIF5 function. This work highlights the importance of typical and atypical bHLH transcription regulators for the integration of light signals from different photoreceptors and provides further mechanistic insight into the crosstalk of UVR8 signaling and SAS.
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Project description:Shade avoidance response (S.A.R) is regulated by light and circadian clock. Circadian clock controls S.A.R by the transcriptional regulation of positive regulators of S.A.R, PIF4 and PIF5, to prevent plants from responding to 'light' of dark period. Thus, in many cases, deficits in circadian clock appear in abnormalities of hypocotyl and/or petiole elongation. Previously, interesting phenomena were reported that the triple mutants of PSEUDO RESPONSE REGULATORS9, 7 and 5, which are clock components, show longer petioles and smaller leaves under light/dark cycle than those under continuous lighting. These S.A.R-like phenotypes cannot be explained by their hyposensitivity to red light. We demonstrated detailed analyses of this mutant to reveal the leaf-specific S.A.R regulated by circadian clock. Expression analyses of S.A.R-related genes suggested that PRR5 functions as a repressor of S.A.R. Morphological analyses of leaves under different light condition revealed that PRR5 is involved in the inhibition of leaf expansion in S.A.R.
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