The Arabidopsis thaliana genome encodes 29 AT-HOOK MOTIF CONTAINING NUCLEAR LOCALIZED (AHL) genes, which evolved into two phylogenic clades. The AHL proteins contain one or two AT-hook motif(s) and one plant and prokaryote conserved (PPC)/domain of unknown function #296 (DUF296) domain. Seedlings lacking both SOB3/AHL29 and ESC/AHL27 confer a subtle long-hypocotyl phenotype compared with the WT or either single-null mutant. In contrast, the missense allele sob3-6 confers a dramatic long-hypocotyl phenotype in the light. In this study, we examined the dominant-negative feature of sob3-6 and found that it encodes a protein with a disrupted AT-hook motif that abolishes binding to AT-rich DNA. A loss-of-function approach demonstrated different, yet redundant, contributions of additional AHL genes in suppressing hypocotyl elongation in the light. We showed that AHL proteins interact with each other and themselves via the PPC/DUF296 domain. AHLs also share interactions with other nuclear proteins, such as transcription factors, suggesting that these interactions also contribute to the functional redundancy within this gene family. The coordinated action of AHLs requires an AT-hook motif capable of binding AT-rich DNA, as well as a PPC/DUF296 domain containing a conserved Gly-Arg-Phe-Glu-Ile-Leu region. Alteration of this region abolished SOB3/AHL29's physical interaction with transcription factors and resulted in a dominant-negative allele in planta that was phenotypically similar to sob3-6. We propose a molecular model where AHLs interact with each other and themselves, as well as other nuclear proteins, to form complexes which modulate plant growth and development.enhanceosome | seedling establishment
Plants reprogram somatic cells following injury and regenerate new tissues and organs. Upon perception of inductive cues, somatic cells often dedifferentiate, proliferate, and acquire new fates to repair damaged tissues or develop new organs from wound sites. Wound stress activates transcriptional cascades to promote cell fate reprogramming and initiate new developmental programs. Wounding also modulates endogenous hormonal responses by triggering their biosynthesis and/or directional transport. Auxin and cytokinin play pivotal roles in determining cell fates in regenerating tissues and organs. Exogenous application of these plant hormones enhances regenerative responses in vitro by facilitating the activation of specific developmental programs. Many reprogramming regulators are epigenetically silenced during normal development but are activated by wound stress and/or hormonal cues.
BackgroundMembers of the ancient land-plant-specific transcription factor AT-Hook Motif Nuclear Localized (AHL) gene family regulate various biological processes. However, the relationships among the AHL genes, as well as their evolutionary history, still remain unexplored.ResultsWe analyzed over 500 AHL genes from 19 land plant species, ranging from the early diverging Physcomitrella patens and Selaginella to a variety of monocot and dicot flowering plants. We classified the AHL proteins into three types (Type-I/-II/-III) based on the number and composition of their functional domains, the AT-hook motif(s) and PPC domain. We further inferred their phylogenies via Bayesian inference analysis and predicted gene gain/loss events throughout their diversification. Our analyses suggested that the AHL gene family emerged in embryophytes and further evolved into two distinct clades, with Type-I AHLs forming one clade (Clade-A), and the other two types together diversifying in another (Clade-B). The two AHL clades likely diverged before the separation of Physcomitrella patens from the vascular plant lineage. In angiosperms, Clade-A AHLs expanded into 5 subfamilies; while, the ones in Clade-B expanded into 4 subfamilies. Examination of their expression patterns suggests that the AHLs within each clade share similar expression patterns with each other; however, AHLs in one monophyletic clade exhibit distinct expression patterns from the ones in the other clade. Over-expression of a Glycine max AHL PPC domain in Arabidopsis thaliana recapitulates the phenotype observed when over-expressing its Arabidopsis thaliana counterpart. This result suggests that the AHL genes from different land plant species may share conserved functions in regulating plant growth and development. Our study further suggests that such functional conservation may be due to conserved physical interactions among the PPC domains of AHL proteins.ConclusionsOur analyses reveal a possible evolutionary scenario for the AHL gene family in land plants, which will facilitate the design of new studies probing their biological functions. Manipulating the AHL genes has been suggested to have tremendous effects in agriculture through increased seedling establishment, enhanced plant biomass and improved plant immunity. The information gleaned from this study, in turn, has the potential to be utilized to further improve crop production.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-014-0266-7) contains supplementary material, which is available to authorized users.
Wounding triggers organ regeneration in many plant species, and application of plant hormones, such as auxin and cytokinin, enhances their regenerative capacities in tissue culture. Recent studies have identified several key players mediating wound- and/or plant hormone-induced cellular reprogramming, but the global architecture of gene regulatory relationships underlying plant cellular reprogramming is still far from clear. In this study, we uncovered a gene regulatory network (GRN) associated with plant cellular reprogramming by using an enhanced yeast one-hybrid (eY1H) screen systematically to identify regulatory relationships between 252 transcription factors (TFs) and 48 promoters. Our network analyses suggest that wound- and/or hormone-invoked signals exhibit extensive cross-talk and regulate many common reprogramming-associated genes via multilayered regulatory cascades. Our data suggest that PLETHORA 3 (PLT3), ENHANCER OF SHOOT REGENERATION 1 (ESR1) and HEAT SHOCK FACTOR B 1 (HSFB1) act as critical nodes that have many overlapping targets and potentially connect upstream stimuli to downstream developmental decisions. Interestingly, a set of wound-inducible APETALA 2/ETHYLENE RESPONSE FACTORs (AP2/ERFs) appear to regulate these key genes, which, in turn, form feed-forward cascades that control downstream targets associated with callus formation and organ regeneration. In addition, we found another regulatory pathway, mediated by LATERAL ORGAN BOUNDARY/ASYMMETRIC LEAVES 2 (LOB/AS2) TFs, which probably plays a distinct but partially overlapping role alongside the AP2/ERFs in the putative gene regulatory cascades. Taken together, our findings provide the first global picture of the GRN governing plant cell reprogramming, which will serve as a valuable resource for future studies.
Developing seedlings are well equipped to alter their growth in response to external factors in order to maximize their chances of survival. SUPPRESSOR OF PHYTOCHROME B4-#3 (SOB3) and other members of the AT-HOOK MOTIF CONTAINING NUCLEAR LOCALIZED (AHL) family of transcription factors modulate the development of Arabidopsis (Arabidopsis thaliana) by repressing hypocotyl elongation in young seedlings growing in light. However, the molecular mechanism behind how AHLs influence seedling development is largely unknown. We have identified genes associated with auxin-mediated hypocotyl elongation as downstream targets of SOB3. We found that YUCCA8 (YUC8) as well as members of the SMALL AUXIN UP-REGULATED RNA19 (SAUR19) subfamily were down-regulated in the short-hypocotyl, gain-of-function SOB3-D mutant and up-regulated in the dominant-negative, tall-hypocotyl sob3-6 mutant. SOB3-D and sob3-6 hypocotyls also exhibited altered sensitivity to the polar auxin transport inhibitor N-1-napthylphthalamic acid, suggesting a critical connection between auxin and the modulation of seedling elongation by SOB3. Finally, we found that overexpression of GREEN FLUORESCENT PROTEIN-SAUR19 in the SOB3-D line partially rescued defects in hypocotyl elongation, and SOB3 bound directly to the promoters of YUC8 and SAUR19 subfamily members. Taken together, these data indicate that SOB3 modulates hypocotyl elongation in young seedlings by directly repressing the transcription of genes associated with auxin signaling.
Plant somatic cells reprogram and regenerate new tissues or organs when they are severely damaged. These physiological processes are associated with dynamic transcriptional responses but how chromatin-based regulation contributes to wound-induced gene expression changes and subsequent cellular reprogramming remains unknown. In this study we investigate the temporal dynamics of the histone modifications H3K9/14ac, H3K27ac, H3K4me3, H3K27me3, and H3K36me3, and analyze their correlation with gene expression at early time points after wounding. We show that a majority of the few thousand genes rapidly induced by wounding are marked with H3K9/14ac and H3K27ac before and/or shortly after wounding, and these include key wound-inducible reprogramming genes such as WIND1, ERF113/RAP2.6 L and LBD16. Our data further demonstrate that inhibition of GNAT-MYSTmediated histone acetylation strongly blocks wound-induced transcriptional activation as well as callus formation at wound sites. This study thus uncovered a key epigenetic mechanism that underlies wound-induced cellular reprogramming in plants.
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