SummaryFruit development is usually triggered by ovule fertilization, and it requires coordination between seed development and the growth and differentiation of the ovary to host the seeds. Hormones are known to synchronize these two processes, but the role of each hormone, and the mechanism by which they interact, are still unknown. Here we show that auxin and gibberellins (GAs) act in a hierarchical scheme. The synthetic reporter construct DR5:GFP showed that fertilization triggered an increase in auxin response in the ovules, which could be mimicked by blocking polar auxin transport. As the application of GAs did not affect auxin response, the most likely sequence of events after fertilization involves auxin-mediated activation of GA synthesis. We have confirmed this, and have shown that GA biosynthesis upon fertilization is localized specifically in the fertilized ovules. Furthermore, auxin treatment caused changes in the expression of GA biosynthetic genes similar to those triggered by fertilization, and also restricted to the ovules. Finally, GA signaling was activated in ovules and valves, as shown by the rapid downregulation of the fusion protein RGA-GFP after pollination and auxin treatment. Taken together, this evidence suggests a model in which fertilization would trigger an auxin-mediated promotion of GA synthesis specifically in the ovule. The GAs synthesized in the ovules would be then transported to the valves to promote GA signaling and thus coordinate growth of the silique.
Control of tissue dimensions in multicellular organisms requires the precise quantitative regulation of mitotic activity. In plants, where cells are immobile, tissue size is achieved through control of both cell division orientation and mitotic rate. The bHLH transcription factor heterodimer formed by target of monopteros5 (TMO5) and lonesome highway (LHW) is a central regulator of vascular width-increasing divisions. An important unanswered question is how its activity is limited to specify vascular tissue dimensions. Here we identify a regulatory network that restricts TMO5/LHW activity. We show that thermospermine synthase ACAULIS5 antagonizes TMO5/LHW activity by promoting the accumulation of SAC51-LIKE (SACL) bHLH transcription factors. SACL proteins heterodimerize with LHW-therefore likely competing with TMO5/LHW interactions-prevent activation of TMO5/LHW target genes, and suppress the over-proliferation caused by excess TMO5/LHW activity. These findings connect two thus-far disparate pathways and provide a mechanistic understanding of the quantitative control of vascular tissue growth.
The pistil is the specialized plant organ that enables appropriate pollination and ovule fertilization, after which it undergoes growth and differentiation to become a fruit. However, in most species, if ovules are not fertilized around anthesis the pistil irreversibly loses its growth capacity. We used physiological, molecular, and transcriptomic tools to characterize the postanthesis development of the unfertilized Arabidopsis (Arabidopsis thaliana) pistil. Surprisingly, developmental processes that have been previously described in developing Arabidopsis fruits, such as the collapse of the adaxial epidermis, differentiation of a sclerenchyma layer in the adaxial subepidermis and the dehiscence zone, and valve dehiscence, were also observed in the unfertilized pistil. We determined that senescence is first established in the transmitting tract, stigma, and ovules immediately after anthesis, and that the timing of senescence in the stigma and ovules correlates with the loss of fruit-set responsiveness of the pistil to pollen and the hormone gibberellin (GA), respectively. Moreover, we showed that mutants with altered ovule development have impaired fruit-set response to the GA gibberellic acid, which further indicates that the presence of viable ovules is required for fruit-set responsiveness to GAs in the unfertilized pistil. Our data suggest that a fertilizationindependent developmental program controls many of the processes during post-anthesis development, both in unfertilized pistils and seeded fruits, and point to a key role of the ovule in the capacity of pistils to undergo fruit set in response to GA.
SUMMARY Gibberellins (GAs) play a critical role in fruit-set and fruit growth. Gibberellin is perceived by its nuclear receptors GA INSENSITIVE DWARF1s (GID1s), which then trigger degradation of downstream repressors DELLAs. To understand the role of the three GA receptor genes (GID1A, GID1B and GID1C) in Arabidopsis during fruit initiation, we have examined their temporal and spatial localization, in combination with analysis of mutant phenotypes. Distinct expression patterns are revealed for each GID1: GID1A is expressed throughout the whole pistil, while GID1B is expressed in ovules, and GID1C is expressed in valves. Functional study of gid1 mutant combinations confirms that GID1A plays a major role during fruit-set and growth, whereas GID1B and GID1C have specific roles in seed development and pod elongation, respectively. Therefore, in ovules, GA perception is mediated by GID1A and GID1B, while GID1A and GID1C are involved in GA perception in valves. To identify tissue-specific interactions between GID1s and DELLAs, we analyzed spatial expression patterns of four DELLA genes that have a role in fruit initiation (GAI, RGA, RGL1 and RGL2). Our data suggest that GID1A can interact with RGA and GAI in all tissues, whereas GID1C–RGL1 and GID1B–RGL2 interactions only occur in valves and ovules, respectively. These results uncover specific functions of each GID1–DELLA in the different GA-dependent processes that occur upon fruit-set. In addition, the distribution of GA receptors in valves along with lack of expression of GA biosynthesis genes in this tissue, strongly suggests transport of GAs from the developing seeds to promote fruit growth.
BackgroundOvule lifespan is an important factor in determining the ability to set fruits and produce seeds. Once ovule senescence is established, fruit set capacity in response to gibberellins (GAs) is lost. We aimed to elucidate whether ethylene plays a role in controlling ovule senescence and the fruit set response in Arabidopsis.ResultsEthylene response inhibitors, silver thiosulphate (STS) and 1-methylcyclopropene (1-MCP), were able to delay the loss of pistil response to GA3. In addition, ethylene insensitive mutants ein2-5 and ein3-1 showed delayed loss of pistil response, as in plants treated with STS and 1-MCP, while constitutive mutant ctr1-1 displayed premature loss of response. The analysis of the expression of ethylene biosynthesis genes suggests that ethylene is synthesised in ovules at the onset of ovule senescence, while a transcriptional meta-analysis also supports an activated ethylene-dependent senescence upon the establishment of ovule senescence. Finally, a SAG12:GUS reporter line proved useful to monitor ovule senescence and to directly demonstrate that ethylene specifically modulates ovule senescence.ConclusionsWe have shown that ethylene is involved in both the control of the ovule lifespan and the determination of the pistil/fruit fate. Our data support a role of the ovule in modulating the GA response during fruit set in Arabidopsis. A possible mechanism that links the ethylene modulation of the ovule senescence and the GA3-induced fruit set response is discussed.
Although originally identified as the components of the complex aiding the cytosolic chaperonin CCT in the folding of actins and tubulins in the cytosol, prefoldins (PFDs) are emerging as novel regulators influencing gene expression in the nucleus. Work conducted mainly in yeast and animals showed that PFDs act as transcriptional regulators and participate in the nuclear proteostasis. To investigate new functions of PFDs, we performed a co-expression analysis in Arabidopsis thaliana. Results revealed co-expression between PFD and the Sm-like (LSM) genes, which encode the LSM2–8 spliceosome core complex, in this model organism. Here, we show that PFDs interact with and are required to maintain adequate levels of the LSM2–8 complex. Our data indicate that levels of the LSM8 protein, which defines and confers the functional specificity of the complex, are reduced in pfd mutants and in response to the Hsp90 inhibitor geldanamycin. We provide biochemical evidence showing that LSM8 is a client of Hsp90 and that PFD4 mediates the interaction between both proteins. Consistent with our results and with the role of the LSM2–8 complex in splicing through the stabilization of the U6 snRNA, pfd mutants showed reduced levels of this snRNA and altered pre-mRNA splicing patterns.
The thickening of plant organs is supported by secondary growth, a process by which new vascular tissues (xylem and phloem) are produced. Xylem is composed of several cell types, including xylary fibers, parenchyma and vessel elements. In Arabidopsis, it has been shown that fibers are promoted by the class-I KNOX gene KNAT1 and the plant hormones gibberellins, and are repressed by a small set of receptor-like kinases; however, we lack a mechanistic framework to integrate their relative contributions. Here, we show that DELLAs, negative elements of the gibberellin signaling pathway, physically interact with KNAT1 and impair its binding to KNAT1-binding sites. Our analysis also indicates that at least 37% of the transcriptome mobilized by KNAT1 is potentially dependent on this interaction, and includes genes involved in secondary cell wall modifications and phenylpropanoid biosynthesis. Moreover, the promotion by constitutive overexpression of KNAT1 of fiber formation and the expression of genes required for fiber differentiation were still reverted by DELLA accumulation, in agreement with post-translational regulation of KNAT1 by DELLA proteins. These results suggest that gibberellins enhance fiber development by promoting KNAT1 activity.
In plants, secondary growth results in radial expansion of stems and roots, generating large amounts of biomass in the form of wood. Using genome-wide association studies (GWAS)-guided reverse genetics inArabidopsis thaliana, we discoveredSOBIR1/EVR, previously known to control plant immunoresponses and abscission, as a regulator of secondary growth. We present anatomical, genetic, and molecular evidence indicating that SOBIR1/EVR prevents the precocious differentiation of xylem fiber, a key cell type for wood development. SOBIR1/EVR acts through a mechanism that involves BREVIPEDICELLUS (BP) and ERECTA (ER), 2 proteins previously known to regulate xylem fiber development. We demonstrate that BP bindsSOBIR1/EVRpromoter and thatSOBIR1/EVRexpression is enhanced inbpmutants, suggesting a direct, negative regulation of BP overSOBIR1/EVRexpression. We show that SOBIR1/EVR physically interacts with ER and that defects caused by thesobir1/evrmutation are aggravated by mutatingER, indicating that SOBIR1/EVR and ERECTA act together in the control of the precocious formation of xylem fiber development.
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