Structural organization of organs in multicellular organisms occurs through intricate patterning mechanisms that often involve complex interactions between transcription factors in regulatory networks. For example, INDEHISCENT (IND), a basic helix-loop-helix (bHLH) transcription factor, specifies formation of the narrow stripes of valve margin tissue, where Arabidopsis thaliana fruits open on maturity. Another bHLH transcription factor, SPATULA (SPT), is required for reproductive tissue development from carpel margins in the Arabidopsis gynoecium before fertilization. Previous studies have therefore assigned the function of SPT to early gynoecium stages and IND to later fruit stages of reproductive development. Here we report that these two transcription factors interact genetically and via protein-protein contact to mediate both gynoecium development and fruit opening. We show that IND directly and positively regulates the expression of SPT, and that spt mutants have partial defects in valve margin formation. Careful analysis of ind mutant gynoecia revealed slight defects in apical tissue formation, and combining mutations in IND and SPT dramatically enhanced both single-mutant phenotypes. Our data show that SPT and IND at least partially mediate their joint functions in gynoecium and fruit development by controlling auxin distribution and suggest that this occurs through cooperative binding to regulatory sequences in downstream target genes.

Monocarpic plants have a single reproductive cycle in their lives, where life span is determined by the coordinated arrest of all meristems, or global proliferative arrest (GPA). The molecular bases for GPA and the signaling mechanisms involved are poorly understood, other than systemic cues from developing seeds of unknown nature. Here we uncover a genetic pathway regulating GPA in Arabidopsis that responds to age-dependent factors and acts in parallel to seed-derived signals. We show that FRUITFULL (FUL), a MADS-box gene involved in flowering and fruit development, has a key role in promoting meristem arrest, as GPA is delayed and fruit production is increased in ful mutants. FUL directly and negatively regulates APETALA2 expression in the shoot apical meristem and maintains the temporal expression of WUSCHEL which is an essential factor for meristem maintenance.

SummaryFRUITFULL is uncovered as a modulator of the function of flowering time integrators, highlighting the importance of protein–protein complexes in the fine-tuning of the flowering time response.

The study of floral organ development has been a driving force in plant developmental biology research for the last two decades, and there is now an enormous wealth of information about the genetic networks underlying the specification of floral organ identity and the acquisition of its final morphology and function. These and parallel studies on leaf morphogenesis and development have made evident the common evolutionary origin of all plant lateral organs and the recurrent use of variations in the regulatory circuits involved in the shaping of leaves and flowers. This review summarizes the latest progress on the study of the development of the gynoecium, the female reproductive organ of the flower, stressing the connections with the developmental programme of leaf morphogenesis, and highlighting the common role of hormonal cues in these processes.

The four NGATHA genes (NGA) form a small subfamily within the large family of B3-domain transcription factors of Arabidopsis thaliana. NGA genes act redundantly to direct the development of the apical tissues of the gynoecium, the style, and the stigma. Previous studies indicate that NGA genes could exert this function at least partially by directing the synthesis of auxin at the distal end of the developing gynoecium through the upregulation of two different YUCCA genes, which encode flavin monooxygenases involved in auxin biosynthesis. We have compared three developing pistil transcriptome data sets from wildtype, nga quadruple mutants, and a 35S::NGA3 line. The differentially expressed genes showed a significant enrichment for auxin-related genes, supporting the idea of NGA genes as major regulators of auxin accumulation and distribution within the developing gynoecium. We have introduced reporter lines for several of these differentially expressed genes involved in synthesis, transport and response to auxin in NGA gain- and loss-of-function backgrounds. We present here a detailed map of the response of these reporters to NGA misregulation that could help to clarify the role of NGA in auxin-mediated gynoecium morphogenesis. Our data point to a very reduced auxin synthesis in the developing apical gynoecium of nga mutants, likely responsible for the lack of DR5rev::GFP reporter activity observed in these mutants. In addition, NGA altered activity affects the expression of protein kinases that regulate the cellular localization of auxin efflux regulators, and thus likely impact auxin transport. Finally, protein accumulation in pistils of several ARFs was differentially affected by nga mutations or NGA overexpression, suggesting that these accumulation patterns depend not only on auxin distribution but could be also regulated by transcriptional networks involving NGA factors.

SUMMARYFruits are complex plant structures that nurture seeds and facilitate their dispersal. The Arabidopsis fruit is termed silique. It develops from the gynoecium, which has a stigma, a style, an ovary containing the ovules, and a gynophore. Externally, the ovary consists of two valves, and their margins lay adjacent to the replum, which is connected to the septum that internally divides the ovary. In this work we describe the role for the zinc-finger transcription factor NO TRANSMITTING TRACT (NTT) in replum development. NTT loss of function leads to reduced replum width and cell number, whereas increased expression promotes replum enlargement. NTT activates the homeobox gene BP, which, together with RPL, is important for replum development. In addition, the NTT protein is able to bind the BP promoter in yeast, and when this binding region is not present, NTT fails to activate BP in the replum. Furthermore, NTT interacts with itself and different proteins involved in fruit development: RPL, STM, FUL, SHP1 and SHP2 in yeast and in planta. Moreover, its genetic interactions provide further evidence about its biological relevance in replum development.

Seed dispersal is an essential trait that enables colonization of new favorable habitats, ensuring species survival. In plants with dehiscent fruits, such as Arabidopsis, seed dispersal depends on two processes: the separation of the fruit valves that protect the seeds (fruit dehiscence) and the detachment of the seeds from the funiculus connecting them to the mother plant (seed abscission). The key factors required to establish a proper lignin pattern for fruit dehiscence are SHATTERPROOF 1 and 2 (SHP1 and SHP2). Here, we demonstrate that the SHP-related gene SEEDSTICK (STK) is a key factor required to establish the proper lignin pattern in the seed abscission zone but in an opposite way. We show that STK acts as a repressor of lignin deposition in the seed abscission zone through the direct repression of HECATE3, whereas the SHP proteins promote lignin deposition in the valve margins by activating INDEHISCENT. The interaction of STK with the SEUSS co-repressor determines the difference in the way STK and SHP proteins control the lignification patterns. Despite this difference in the molecular control of lignification during seed abscission and fruit dehiscence, we show that the genetic networks regulating these two developmental pathways are highly conserved.

Upon fertilization, the ovary increases in size and undergoes a complex developmental process to become a fruit. We show that cytokinins (CKs), which are required to determine ovary size before fertilization, have to be degraded to facilitate fruit growth. The expression of CKX7, which encodes a cytosolic CK-degrading enzyme, is directly positively regulated post-fertilization by the MADS-box transcription factor STK. Similar to stk, two ckx7 mutants possess shorter fruits than wild type. Quantification of CKs reveals that stk and ckx7 mutants have high CK levels, which negatively control cell expansion during fruit development, compromising fruit growth. Overexpression of CKX7 partially complements the stk fruit phenotype, confirming a role for CK degradation in fruit development. Finally, we show that STK is required for the expression of FUL, which is essential for valve elongation. Overall, we provide insights into the link between CKs and molecular pathways that control fruit growth.