Significance: Various plant organs respond differentially to environmental signals so that plants can adapt to dynamic environments without movement. Light is a key environmental factor mediating multiple plant developmental processes. For example, it induces cotyledon expansion but inhibits hypocotyl elongation when plants emerge from soil. Although this opposite regulation is crucial for plant survival and has been described for decades, the underlying mechanism is still elusive. In this study, we demonstrated that temporal–spatial expression of a group of Small Auxin Up RNA s ( SAUR s) is regulated by light through auxin and phytochrome-interacting factors, and these SAURs further mediate the differential growth of cotyledons and hypocotyls. Thus, this study provides a molecular mechanism explaining how light differentially regulates the growth of various plant organs.

Arabidopsis thaliana seedlings undergo photomorphogenic development even in darkness when the function of DE-ETIOLATED1 (DET1), a repressor of photomorphogenesis, is disrupted. However, the mechanism by which DET1 represses photomorphogenesis remains unclear. Our results indicate that DET1 directly interacts with a group of transcription factors known as the phytochrome-interacting factors (PIFs). Furthermore, our results suggest that DET1 positively regulates PIF protein levels primarily by stabilizing PIF proteins in the dark. Genetic analysis showed that each pif single mutant could enhance the det1-1 phenotype, and ectopic expression of each PIF in det1-1 partially suppressed the det1-1 phenotype, based on hypocotyl elongation and cotyledon opening angles observed in darkness. Genomic analysis also revealed that DET1 may modulate the expression of light-regulated genes to mediate photomorphogenesis partially through PIFs. The observed interaction and regulation between DET1 and PIFs not only reveal how DET1 represses photomorphogenesis, but also suggest a possible mechanism by which two groups of photomorphogenic repressors, CONSTITUTIVE PHOTOMORPHOGENESIS/DET/FUSCA and PIFs, work in concert to repress photomorphogenesis in darkness.

Light elicits different growth responses in different organs of plants. These organ-specific responses are prominently displayed during de-etiolation. While major light-responsive components and early signaling pathways in this process have been identified, this information has yet to explain how organ-specific light responses are achieved. Here, we report that members of the TEOSINTE BRANCHED1, CYCLOIDEA, and PCF (TCP) transcription factor family participate in photomorphogenesis and facilitate light-induced cotyledon opening in Arabidopsis (Arabidopsis thaliana). Chromatin immunoprecipitation sequencing and RNA sequencing analyses indicated that TCP4 targets a number of SMALL AUXIN UPREGULATED RNA (SAUR) genes that have previously been shown to exhibit organ-specific, light-responsive expression. We demonstrate that TCP4-like transcription factors, which are predominantly expressed in the cotyledons of both light- and dark-grown seedlings, activate SAUR16 and SAUR50 expression in response to light. Light regulates the binding of TCP4 to the promoters of SAUR14, SAUR16, and SAUR50 through PHYTOCHROME-INTERACTING FACTORs (PIFs). PIF3, which accumulates in etiolated seedlings and its levels rapidly decline upon light exposure, also binds to the SAUR16 and SAUR50 promoters, while suppressing the binding of TCP4 to these promoters in the dark. Our study reveals that the interplay between light-responsive factors PIFs and the developmental regulator TCP4 determines the cotyledon-specific light regulation of SAUR16 and SAUR50, which contributes to cotyledon closure and opening before and after de-etiolation.

The control of seed germination and seed dormancy are critical for the successful propagation of plant species, and are important agricultural traits. Seed germination is tightly controlled by the balance of gibberellin (GA) and abscisic acid (ABA), and is influenced by environmental factors. The COP9 Signalosome (CSN) is a conserved multi-subunit protein complex that is best known as a regulator of the Cullin-RING family of ubiquitin E3 ligases (CRLs). Multiple viable mutants of the CSN showed poor germination, except for csn5b-1. Detailed analyses showed that csn1-10 has a stronger seed dormancy, while csn5a-1 mutants exhibit retarded seed germination in addition to hyperdormancy. Both csn5a-1 and csn1-10 plants show defects in the timely removal of the germination inhibitors: RGL2, a repressor of GA signaling, and ABI5, an effector of ABA responses. We provide genetic evidence to demonstrate that the germination phenotype of csn1-10 is caused by over-accumulation of RGL2, a substrate of the SCF (CRL1) ubiquitin E3 ligase, while the csn5a-1 phenotype is caused by over-accumulation of RGL2 as well as ABI5. The genetic data are consistent with the hypothesis that CSN5A regulates ABI5 by a mechanism that may not involve CSN1. Transcriptome analyses suggest that CSN1 has a more prominent role than CSN5A during seed maturation, but CSN5A plays a more important role than CSN1 during seed germination, further supporting the functional distinction of these two CSN genes. Our study delineates the molecular targets of the CSN complex in seed germination, and reveals that CSN5 has additional functions in regulating ABI5, thus the ABA signaling pathway. The control of seed germination and seed dormancy are critical for successful propagation of plant species, and manipulation of these processes is important for agriculture. The COP9 Signalosome (CSN) is a multi-subunit protein complex that regulates proteasome-mediated protein degradation in part as a regulator of SCF ubiquitin E3 ligases. The CSN is important for timely germination of seeds, but its molecular targets in this process is unclear. In this study, we demonstrate that the CSN regulates protein stabilities of two different targets from two antagonistic hormonal pathways, RGL2 of the GA pathway and ABI5 of the ABA pathway. Our genetic and transcriptome analyses showed that, although csn1-10 and csn5a-1 exhibit similar defects in timely germination, the mechanisms of how the mutations affect seed germination differ. Since RGL2 is known to be targeted by SCF during germination, the defect in the timely degradation of RGL2 in csn1-10 and csn5a-1 is consistent with the role of CSN as a regulator of the SCF. In addition, we show that CSN5A, but not CSN1, has an additional function in regulating ABI5, a downstream inhibitor of germination.

The tail of replication-dependent histone H3.1 varies from that of replication-independent H3.3 at the amino acid located at position 31 in plants and animals, but no function has been assigned to this residue to demonstrate a unique and conserved role for H3.1 during replication. We found that TONSOKU (TSK/TONSL), which rescues broken replication forks, specifically interacts with H3.1 via recognition of alanine 31 by its tetratricopeptide repeat domain. Our results indicate that genomic instability in the absence of ATXR5/ATXR6-catalyzed histone H3 lysine 27 monomethylation in plants depends on H3.1, TSK, and DNA polymerase theta (Pol θ). This work reveals an H3.1-specific function during replication and a common strategy used in multicellular eukaryotes for regulating post-replicative chromatin maturation and TSK, which relies on histone monomethyltransferases and reading of the H3.1 variant.

The phytochrome B (phyB) photoreceptor stimulates light responses in plants in part by inactivating repressors of light responses, such as PHYTOCHROME-INTERACTING FACTOR3 (PIF3). Activated phyB inhibits PIF3 by rapid protein degradation and decreased transcription. PIF3 protein degradation is mediated by EIN3-BINDING F-BOX PROTEIN (EBF) and LIGHT-RESPONSE BTB (LRB) E3 ligases, the latter of which simultaneously targets phyB for degradation. In this study, we show that PIF3 levels are additionally regulated by alternative splicing and protein translation in Arabidopsis (Arabidopsis thaliana). Overaccumulation of photo-activated phyB, which occurs in the mutant defective for LRB genes under continuous red light, induces a specific alternative splicing of PIF3 that results in retention of an intron in the 5′ untranslated region of PIF3 mRNA. In turn, the upstream open reading frames contained within this intron inhibit PIF3 protein synthesis. The phyB-dependent alternative splicing of PIF3 is diurnally regulated under the short-day light cycle. We hypothesize that this reversible regulatory mechanism may be utilized to fine tune the level of PIF3 protein in light-grown plants and may contribute to the oscillation of PIF3 protein abundance under the short-day environment.