Carpels are essential for sexual plant reproduction because they house the ovules and subsequently develop into fruits that protect, nourish and ultimately disperse the seeds. The AGAMOUS (AG) gene is necessary for plant sexual reproduction because stamens and carpels are absent from ag mutant flowers. However, the fact that sepals are converted into carpelloid organs in certain mutant backgrounds even in the absence of AG activity indicates that an AG-independent carpel-development pathway exists. AG is a member of a monophyletic clade of MADS-box genes that includes SHATTERPROOF1 (SHP1), SHP2 and SEEDSTICK (STK), indicating that these four genes might share partly redundant activities. Here we show that the SHP genes are responsible for AG-independent carpel development. We also show that the STK gene is required for normal development of the funiculus, an umbilical-cord-like structure that connects the developing seed to the fruit, and for dispersal of the seeds when the fruit matures. We further show that all four members of the AG clade are required for specifying the identity of ovules, the landmark invention during the course of vascular plant evolution that enabled seed plants to become the most successful group of land plants.
The fruit, which mediates the maturation and dispersal of seeds, is a complex structure unique to flowering plants. Seed dispersal in plants such as Arabidopsis occurs by a process called fruit dehiscence, or pod shatter. Few studies have focused on identifying genes that regulate this process, in spite of the agronomic value of controlling seed dispersal in crop plants such as canola. Here we show that the closely related SHATTERPROOF (SHP1) and SHATTERPROOF2 (SHP2) MADS-box genes are required for fruit dehiscence in Arabidopsis. Moreover, SHP1 and SHP2 are functionally redundant, as neither single mutant displays a novel phenotype. Our studies of shp1 shp2 fruit, and of plants constitutively expressing SHP1 and SHP2, show that these two genes control dehiscence zone differentiation and promote the lignification of adjacent cells. Our results indicate that further analysis of the molecular events underlying fruit dehiscence may allow genetic manipulation of pod shatter in crop plants.
The Arabidopsis seedpod opens through a spring-loaded mechanism known as pod shatter, which is essential for dispersal of the seeds. Here, we identify INDEHISCENT (IND), an atypical bHLH protein, that is necessary for fruit opening and is involved in patterning each of the three fruit cell types required for seed dispersal. Previous studies suggested that FRUITFULL (FUL), a member of the MADS-domain transcription factor family, is required for fruit growth since ful mutant fruit fail to undergo the dramatic enlargement that normally occurs after fertilization. Here we show, however, that FUL is not directly required for fruit elongation and instead is required to prevent ectopic activity of IND. Our molecular and genetic studies suggest a model for the regulatory interactions among the genes that control fruit development and the mechanism that results in the expression of IND in a narrow stripe of cells.
Changes in genes encoding transcriptional regulators can alter development and are important components of the molecular mechanisms of morphological evolution. MADS-box genes encode transcriptional regulators of diverse and important biological functions. In plants, MADS-box genes regulate flower, fruit, leaf, and root development. Recent sequencing efforts in Arabidopsis have allowed a nearly complete sampling of the MADS-box gene family from a single plant, something that was lacking in previous phylogenetic studies. To test the long-suspected parallel between the evolution of the MADS-box gene family and the evolution of plant form, a polarized gene phylogeny is necessary. MEF2 ͉ SRF ͉ homeotic genes ͉ MADS ͉ development C hanges in genes encoding transcriptional regulators may represent the most important determinants of morphological evolution in plants and animals (1), and phylogenetic analyses provide a historical framework to identify such changes. The MADS-box genes encode a eukaryotic family of transcriptional regulators involved in diverse and important biological functions, ranging from cardiac muscle development in animals to pheromone response in yeast (2). In plants, MADS-box genes encode the three floral homeotic functions predicted by the genetic ABC model of flower organ identity (3, 4). In addition, plant MADS-box genes regulate the timing of flower initiation and flower meristem identity, as well as various aspects of ovule, fruit, leaf, and root development (4, 5).Previously identified plant MADS-box genes encode proteins that share a stereotypical MIKC structure (Fig. 1), with the highly conserved DNA-binding MADS domain at the amino terminus. The moderately conserved K domain in the central portion of these proteins has been shown to be important for protein-protein interactions and likely forms a coiled-coil structure. The MADS and K domains are linked to one another by a weakly conserved I domain, whereas a poorly conserved carboxyl-terminal (C) region may function as a trans-activation domain (4). In animals and fungi, two distinct types of MADSbox genes have been identified, the SRF-like and MEF2-like classes (ref. 2; see Fig. 1).This paper provides a hypothesis on the evolutionary history of the eukaryotic MADS-box gene family. Previous studies of eukaryotic MADS-box gene evolution, which included plant and animal sequences, provided unrooted trees useful to infer the phylogenetic relationships of the MADS-box lineages (6). These previous studies suggested that at least one MADS-box gene was present in the common ancestor of plants, animals, and fungi, and that probably the duplication that gave rise to the animal MEF2-and SRF-like genes occurred after animals diverged from plants but before fungi diverged from animals (6). However, previous plant and eukaryotic studies were based on a relatively small sampling of plant MADS-box sequences for a particular species (6-9). To test whether all Arabidopsis MADSbox sequences group in a monophyletic clade distinct from all animal and fungal ...
The terminal step of fruit development in Arabidopsis involves valve separation from the replum, allowing seed dispersal. This process requires the activities of the SHATTERPROOF MADS-box genes, which promote dehiscence zone differentiation at the valve/replum boundary. Here we show that the FRUITFULL MADS-box gene, which is necessary for fruit valve differentiation, is a negative regulator of SHATTERPROOF expression and that constitutive expression of FRUITFULL is sufficient to prevent formation of the dehiscence zone. Our studies suggest that ectopic expression of FRUITFULL may directly allow the control of pod shatter in oilseed crops such as canola.
During senescence, chlorophyll (chl) is metabolized to colorless nonfluorescent chl catabolites (NCCs). A central reaction of the breakdown pathway is the ring cleavage of pheophorbide (pheide) a to a primary fluorescent chl catabolite. Two enzymes catalyze this reaction, pheide a oxygenase (PAO) and red chl catabolite reductase. Five NCCs and three fluorescent chl catabolites (FCCs) accumulated during dark-induced chl breakdown in Arabidopsis (Arabidopsis thaliana). Three of these NCCs and one FCC (primary fluorescent chl catabolite-1) were identical to known catabolites from canola (Brassica napus). The presence in Arabidopsis of two modified FCCs supports the hypothesis that modifications, as present in NCCs, occur at the level of FCC. Chl degradation in Arabidopsis correlated with the accumulation of FCCs and NCCs, as well as with an increase in PAO activity. This increase was due to an up-regulation of Pao gene expression. In contrast, red chl catabolite reductase is not regulated during leaf development and senescence. A pao1 knockout mutant was identified and analyzed. The mutant showed an age-and light-dependent cell death phenotype on leaves and in flowers caused by the accumulation of photoreactive pheide a. In the dark, pao1 exhibited a stay-green phenotype. The key role of PAO in chl breakdown is discussed.Chlorophyll (chl) degradation is an integral part of leaf senescence and fruit ripening. The fate of chl during senescence has been well established in recent years (for review, see Matile et al., 1999; Hörtensteiner, 1999; Hö rtensteiner and Kräutler, 2000;Kräutler, 2003;Eckhardt et al., 2004). Thereby, chl is converted to colorless nonfluorescent chl catabolites (NCCs; Fig. 1) in a pathway that is probably active in all higher plants (Pružinská et al., 2003;Gray et al., 2004). Structure elucidation of NCCs from different species has unraveled a common tetrapyrrolic skeleton with an oxygenolytically opened porphyrin macrocycle (Kräutler, 2003). Peripheral modifications at several side chains within different NCCs (Fig. 1, R 1 -R 3 ) are species specific (Berghold et al., 2002(Berghold et al., , 2004, and hence have been proposed to occur rather late in the pathway (Hö rtensteiner, 1999). Indeed, a primary chl breakdown product (primary fluorescent chl catabolite-1 [pFCC-1]), which exhibits a blue fluorescence, could be identified as a common product of porphyrin ring cleavage ( Fig. 1; Mü hlecker et al., 1997). Thus, the sequence of reactions is the removal of phytol and magnesium (Mg) by chlorophyllase and Mg-dechelatase, respectively, followed by the conversion of pheophorbide (pheide) a to pFCC-1, which requires the activity of two enzymes, pheide a oxygenase (PAO) and red chl catabolite (RCC) reductase (RCCR; Rodoni et al., 1997;Hö rtensteiner, 1999).PAO is a chloroplast envelope-bound Rieske-type iron-sulfur oxygenase, which is identical to lethal leaf spot 1 (LLS1) from maize (Zea mays) and accelerated cell death 1 (ACD1) from Arabidopsis (Arabidopsis thaliana; Pružinská et al., 2003;Yang e...
Local hormone maxima are essential for the development of multicellular structures and organs. For example, steroid hormones accumulate in specific cell types of the animal fetus to induce sexual differentiation and concentration peaks of the plant hormone auxin direct organ initiation and mediate tissue patterning. Here we provide an example of a regulated local hormone minimum required during organogenesis. Our results demonstrate that formation of a local auxin minimum is necessary for specification of the valve margin separation layer where Arabidopsis fruit opening takes place. Consequently, ectopic production of auxin, specifically in valve margin cells, leads to a complete loss of proper cell fate determination. The valve margin identity factor INDEHISCENT (IND) is responsible for forming the auxin minimum by coordinating auxin efflux in separation-layer cells. We propose that the simplicity of formation and maintenance make local hormone minima particularly well suited to specify a small number of cells such as the stripes at the valve margins.
Upon floral induction, the primary shoot meristem of an Arabidopsis plant begins to produce flower meristems rather than leaf primordia on its flanks. Assignment of floral fate to lateral meristems is primarily due to the cooperative activity of the flower meristem identity genes LEAFY (LFY), APETALA1 (AP1), and CAULIFLOWER. We present evidence here that AP1 expression in lateral meristems is activated by at least two independent pathways, one of which is regulated by LFY. In lfy mutants, the onset of AP1 expression is delayed, indicating that LFY is formally a positive regulator of AP1. We have found that AP1, in turn, can positively regulate LFY, because LFY is expressed prematurely in the converted floral meristems of plants constitutively expressing AP1. Shoot meristems maintain an identity distinct from that of flower meristems, in part through the action of genes such as TERMINAL FLOWER1 (TFL1), which bars AP1 and LFY expression from the influorescence shoot meristem. We show here that this negative regulation can be mutual because TFL1 expression is downregulated in plants constitutively expressing AP1. Therefore, the normally sharp phase transition between the production of leaves with associated shoots and formation of the flowers, which occurs upon floral induction, is promoted by positive feedback interactions between LFY and AP1, together with negative interactions of these two genes with TFL1.
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