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Karrikins Enhance Light Responses During Germination and Seedling Development in Arabidopsis Thaliana

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Karrikins Enhance Light Responses During Germination and Seedling Development in Arabidopsis Thaliana Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana David C. Nelsona, Gavin R. Flemattib, Julie-Anne Riseborougha,c, Emilio L. Ghisalbertib, Kingsley W. Dixonc,d, and Steven M. Smitha,b,1 aPlant Energy Biology, bSchool of Biomedical, Biomolecular, and Chemical Sciences, and cPlant Biology, University of Western Australia, Crawley, WA 6009, Australia; and dKings Park and Botanic Garden, West Perth, WA 6005, Australia Edited* by Winslow R. Briggs, Carnegie Institution of Washington, Stanford, CA, and approved February 25, 2010 (received for review October 12, 2009) Karrikins are a class of seed germination stimulants identified in For example, the double B-box zinc finger proteins STH2 and smoke from wildfires. Microarray analysis of imbibed Arabidopsis STH3/LZF1 physically interact with HY5 and act as positive reg- thaliana seeds was performed to identify transcriptional responses ulators of light signaling during early seedling establishment (15– to KAR1 before germination. A small set of genes that are regulated 17). HY5 may serve as an important integration point for light and by KAR1, even when germination is prevented by the absence of hormone signaling because it has been linked to auxin, cytokinin, gibberellin biosynthesis or light, were identified. Light-induced and abscisic acid (ABA) responses; and gibberellin (GA) represses genes, putative HY5-binding targets, and ABRE-like promoter motifs photomorphogenesis in darkness via COP1 by decreasing HY5 were overrepresented among KAR1-up-regulated genes. KAR1 tran- protein accumulation (18–22). siently induced the light signal transduction transcription factor Karrikins (KAR) have been established as a new class of signaling genes HY5 and HYH. Germination of afterripened Arabidopsis seed molecules in smoke from burning vegetation that trigger seed ger- fl was triggered at lower uences of red light when treated with KAR1. mination for many angiosperms (23–26). Although karrikins can Light-dependent cotyledon expansion and inhibition of hypocotyl overcome primary dormancy (PD) in Arabidopsis thaliana seed, the elongation were enhanced in the presence of germination-active effectiveness of KAR on germination varies by ecotype and seed HY5 Arabidopsis 1 karrikins. is important for the hypocotyl elongation, dormancy state: highly dormant seed has reduced response, whereas but not seed germination, response to karrikins. These results reveal the rapid germination rates of nondormant seed can mask any a role for karrikins in priming light responses in the emerging seed- fl PLANT BIOLOGY fl fi positive in uence from karrikin (25). KAR1 does not recover ger- ling, and suggest that the in uence of karrikins on post re ecology mination of the ga1-3 mutant, which has no detectable GA biosyn- may not be limited to germination recruitment. thesis, or enhance its sensitivity to exogenous GAs. Active karrikins induce transcript levels of GA biosynthetic enzymes GA3ox1 and smoke | photomorphogenesis GA3ox2, but there is no corresponding influence on either GA4 or ABA levels during the first 48 h of imbibition. Unlike GAs, karrikins ermination and seedling establishment are critical phases of cannot replace a light requirement for germination (25). Thus, Gthe plant life cycle and are consequently sensitive to a variety of although karrikins require GA biosynthesis to influence germina- external cues, such as light, temperature, and nutrients. Fire events tion, it is unlikely that karrikin responses are exclusively GA- have a dramatic environmental impact that extends beyond imme- mediated. Here, we report an investigation into molecular respon- diate biotic destruction. The reduced competition for resources in ses to KAR that ultimately revealed crosstalk with light-dependent fi 1 the post re environment creates an opportunity for seedling processes during germination and seedling establishment. establishment that is taken advantage of by many species whose germination is recruited by either smoke or heat stimulation (1). Results The reduction of vegetative canopy and ground cover that Identification of KAR -Responsive Genes. To identify molecular re- fi 1 accompanies re also gives rise to changes in the intensity and sponses to karrikin before germination, we used Affymetrix ATH1 spectrum of solar radiation at the soil surface. Both light proper- microarrays to examine transcriptional profiles of the PD seed of fl ties are highly in uential on seed germination and plant devel- the Landsberg erecta (Ler) ecotype imbibed for 24 h in water or 1 opment. The light-regulated control of germination is mediated by μM KAR1. This time point is well before completion of germina- the phytochrome family of photoreceptors, primarily by PhyA and tion, because radicle protrusion was not observed in KAR1-treated PhyB (2). Phytochrome proteins are converted between two iso- seeds at 48 h imbibition and had reached only ∼13% in KAR1- forms by light: an inactive red (R) light absorbing form (Pr) and an treated seeds by 72 h (Fig. S1). It was previously demonstrated that active far-red (FR) light absorbing form (Pfr). The ratio of R:FR is fi fl fi germination of the GA-de cient ga1-3 mutant, which cannot in uenced by canopy ltering, and soil type, moisture, and depth, germinate in the absence of exogenous GAs or other hormone which in turn affects the equilibrium of Pfr:Pr (3, 4). perturbations, is not recovered by KAR1 (25). To identify tran- Substantial work has begun to unravel the complex signal fi fi scriptional changes speci c to KAR1 treatment rather than gen- transduction networks that regulate speci c plant developmental eral germination processes, we also performed an analysis of ga1-3 processes after light is perceived (5, 6). As the hy5 mutant exhibits seed under the same conditions. photomorphogenesis defects under a wide range of light spectra, the bZIP transcription factor ELONGATED HYPOCOTYL5 (HY5) is considered a transducer of light signals from multiple – Author contributions: D.C.N., E.L.G., K.W.D., and S.M.S. designed research; D.C.N., G.R.F., photoreceptors (7 10). Its closest homolog, HYH, has a weaker, and J.-A.R. performed research; G.R.F. contributed new reagents/analytic tools; D.C.N., partially overlapping role that is evident primarily under blue light G.R.F., and J.-A.R. analyzed data; and D.C.N. and S.M.S. wrote the paper. conditions (11). HY5 and HYH are both targeted for degradation The authors declare no conflict of interest. – in the dark by COP1 (11 13). ChIP-chip analysis recently revealed *This Direct Submission article had a prearranged editor. that 14.5% of Arabidopsis gene promoters and an estimated 60% Data deposition: The data reported in this paper have been deposited in the Gene Ex- of early phytochrome-induced gene promoters are putatively pression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. GSE20556). bound by HY5 (14). HY5 does not have a single role in tran- 1To whom correspondence should be addressed. E-mail: [email protected]. scription; its targets may be either activated or repressed in the hy5 This article contains supporting information online at www.pnas.org/cgi/content/full/ mutant (14). HY5 acts with additional transcriptional regulators. 0911635107/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.0911635107 PNAS Early Edition | 1of6 Downloaded by guest on September 25, 2021 We first identified transcriptional changes that were consistent nificant enrichment of both early red and UV-B light-induced genes between both genotypes (Criteria I; Table S1) and then, out of the among KAR-UP transcripts. remaining genes, those that were significantly responsive to KAR1 PIL5 mediates repression of germination in the dark. ChIP-chip in only one genotype (Criteria II; Table S2). A few general was recently used to identify PIL5 binding sites (34). Among KAR- observations can be made from the Criteria I probesets. First, UP genes, 12% had PIL5 binding sites (vs. 3%of genome). Cor- fi KAR1 induced ∼6-fold more transcripts at 24 h than it repressed responding with this, 21% of KAR-UP genes were classi ed as > (Table 1). Second, although the KAR1 treatment substantially repressed by PIL5 (vs. 6%). Thus a 3.5-fold enrichment of PIL5- enhanced PD seed germinability, few “strong” fold changes were regulated genes was observed among those induced by KAR1. observed. Only 30 transcripts were induced at least 2-fold by Finally, we performed an analysis for enriched transcription KAR1, and only one was repressed at least 2-fold (Table 1). Third, factor binding sites among promoters (maximum 1 kb) of KAR-UP the magnitude of transcript induction in response to KAR1 was genes using Athena (40). An Abscisic Acid Response Element largely consistent in PD Ler and ga1-3 seed, despite the disparity in (ABRE)-like binding site motif, (C/G/T)ACGTG(G/T)(A/C), was germination outcome between these genotypes. Of the 118 pro- present in the promoters of 52 (43%) of the 121 genes represented fi besets induced > 1.5-fold by KAR1 in PD Ler, 85 (75%) also had by the 118 probesets. This motif is signi cantly enriched among the FC > 1.5 in ga1-3. Of the 10 most up-regulated transcripts in PD KAR-UP genes when compared against the genome-wide dis- Ler seed, 7 were also among the 10 most up-regulated in ga1-3. tribution of 18%. The ABRE-like binding site motif includes motifs This trend was less notable for down-regulated transcripts, such as ABA-responsive element (ABRE), (C/T)ACGTGGC, and because only 4 probesets (20%) were repressed at least 1.5-fold by the light-responsive element G-box, CACGTG. HY5 has been KAR1 in both genotypes. demonstrated to bind G-box motifs in the promoters of some light- Thus, despite the lack of an overt ga1-3 germination response to regulated genes (7).
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