SUMMARYUnlike the situation in animals, the final morphology of the plant body is highly modulated by the environment. During Arabidopsis development, intrinsic factors provide the framework for basic patterning processes. CLASS III HOMEODOMAIN LEUCINE ZIPPER (HD-ZIPIII) transcription factors are involved in embryo, shoot and root patterning. During vegetative growth HD-ZIPIII proteins control several polarity set-up processes such as in leaves and the vascular system. We have identified several direct target genes of the HD-ZIPIII transcription factor REVOLUTA (REV) using a chromatin immunoprecipitation/DNA sequencing (ChIP-Seq) approach. This analysis revealed that REV acts upstream of auxin biosynthesis and affects directly the expression of several class II HD-ZIP transcription factors that have been shown to act in the shadeavoidance response pathway. We show that, as well as involvement in basic patterning, HD-ZIPIII transcription factors have a critical role in the control of the elongation growth that is induced when plants experience shade. Leaf polarity is established by the opposed actions of HD-ZIPIII and KANADI transcription factors. Finally, our study reveals that the module that consists of HD-ZIPIII/KANADI transcription factors controls shade growth antagonistically and that this antagonism is manifested in the opposed regulation of shared target genes.
In response to plant proximity or canopy shade, plants can react by altering elongation growth and development. Several members of the class II homeodomain-leucine zipper (HD-ZIPII) transcription factor family have been shown to play an instrumental role in the responses to shade. HD-ZIP members of the class III (HD-ZIPIII), by contrast, are involved in basic patterning processes. We recently showed that REVOLUTA (REV), a member of the HD-ZIPIII family, directly and positively regulates the expression of several genes involved in shade-induced growth, such as those encoding HD-ZIPII factors HAT2, HAT3, ATHB2/HAT4 and ATHB4, and of the components of the auxin biosynthesis pathway YUCCA5 and TAA1. Furthermore, we could demonstrate a novel role for HD-ZIPIII in shade-induced promotion of growth. Here we show that besides responding to shade, ATHB4 and HAT3 have a critical role in establishing the dorso-ventral axis in cotyledons and developing leaves. Loss-of-function mutations in these two HD-ZIPII genes (athb4 hat3) results in severely abaxialized, entirely radialized leaves. Conversely, overexpression of HAT3 results in adaxialized leaf development. Taken together, our findings unravel a so far unappreciated role for an HD-ZIPII/HD-ZIPIII module required for dorso-ventral patterning of leaves. The finding that HD-ZIPII/HD-ZIPIII also function in shade avoidance suggests that this module is at the nexus of patterning and growth promotion.
Key messageThe optical brightener SCRI Renaissance 2200 can be used as versatile dye to study various aspects of plant reproduction by confocal laser scanning microscopy.Abstract The study of sexual reproduction of plants has traditionally relied on light microscopy in combination with a variety of staining methods. Transgenic lines that label specific cell or tissue types with fluorescent proteins in combination with confocal laser scanning microscopy were an important development to visualize gametophyte development, the fertilization process, and to follow cell differentiation in the early embryo. Staining the cell perimeter to identify surrounding tissue is often a necessary prerequisite to put the fluorescent signal in the right context. Here, we present SCRI Renaissance 2200 (SR2200) as a versatile dye to study various aspects of plant reproduction ranging from pollen tube growth, guidance and reception to the early patterning process in the developing embryo of Arabidopsis thaliana. Furthermore, we demonstrate that SR2200 can be combined with a wide variety of fluorescent proteins. If spectral information can be recorded, even double labeling with dyes that have very similar emission spectra such as 4′,6-diamidin-2-phenylindol (DAPI) is possible. The presented staining method can be a single, easy-to-use alternative for a range of other staining protocols commonly used for microscopic analyses in plant reproductive biology.Electronic supplementary materialThe online version of this article (doi:10.1007/s00497-015-0267-1) contains supplementary material, which is available to authorized users.
In flowering plants, the asymmetrical division of the zygote is the first hallmark of apical-basal polarity of the embryo and is controlled by a MAP kinase pathway that includes the MAPKKK YODA (YDA). In Arabidopsis, YDA is activated by the membraneassociated pseudokinase SHORT SUSPENSOR (SSP) through an unusual parent-of-origin effect: SSP transcripts accumulate specifically in sperm cells but are translationally silent. Only after fertilization is SSP protein transiently produced in the zygote, presumably from paternally inherited transcripts. SSP is a recently diverged, Brassicaceae-specific member of the BRASSINOSTEROID SIGNALING KINASE (BSK) family. BSK proteins typically play broadly overlapping roles as receptorassociated signaling partners in various receptor kinase pathways involved in growth and innate immunity. This raises two questions: How did a protein with generic function involved in signal relay acquire the property of a signal-like patterning cue, and how is the early patterning process activated in plants outside the Brassicaceae family, where SSP orthologs are absent? Here, we show that Arabidopsis BSK1 and BSK2, two close paralogs of SSP that are conserved in flowering plants, are involved in several YDA-dependent signaling events, including embryogenesis. However, the contribution of SSP to YDA activation in the early embryo does not overlap with the contributions of BSK1 and BSK2. The loss of an intramolecular regulatory interaction enables SSP to constitutively activate the YDA signaling pathway, and thus initiates apical-basal patterning as soon as SSP protein is translated after fertilization and without the necessity of invoking canonical receptor activation.Arabidopsis thaliana | evolution | MAP kinase signaling | embryogenesis |
The first structure that differentiates during plant embryogenesis is the extra-embryonic suspensor that positions the embryo in the lumen of the seed. A central role in nutrient transport has been ascribed to the suspensor in species with prominent suspensor structures. Little is known, however, about what impact the size of the rather simple Arabidopsis (Arabidopsis thaliana) suspensor has on embryogenesis. Here, we describe mutations in the predicted exo-polygalacturonase gene NIMNA (NMA) that lead to cell elongation defects in the early embryo and markedly reduced suspensor length. Mutant nma embryos develop slower than wild-type embryos, and we could observe a similar developmental delay in another mutant with shorter suspensors. Interestingly, for both genes, the paternal allele has a stronger influence on the embryonic phenotype. We conclude that the length of the suspensor is crucial for fast developmental progression of the embryo in Arabidopsis.Annual, self-pollinating weeds such as Arabidopsis (Arabidopsis thaliana) benefit from a short life cycle in their natural ephemeral habitats (Snell and Aarssen, 2005). A rapid progression through embryogenesis is a prerequisite for early seed maturation, and it is therefore not surprising that Arabidopsis sets up its body plan already after a very limited number of cell divisions (Aarssen, 2000;Lau et al., 2012).Arabidopsis embryogenesis starts with the fertilized egg cell, the zygote, which elongates about 3-fold before it divides asymmetrically. The smaller apical cell is the founder of the embryo proper that contributes to most of the later seedling, while the larger basal cell develops into a support structure called the suspensor (Jeong et al., 2011a). The suspensor is formed by a series of transverse cell divisions followed by longitudinal cell expansion forming a stalk-like structure. Only the upper-most suspensor cell, the hypophysis, will contribute to parts of the root meristem, while the rest of the suspensor remains extraembryonic and will cease its growth at the heart stage of the embryo (Yeung and Meinke, 1993). The suspensor is thought to be important for pushing the embryo into the lumen of the seed, where the embryo is surrounded by the nourishing endosperm. In addition, a key function in nutrient and hormone transport to the embryo is assigned to the suspensor (Kawashima and Goldberg, 2010).The Arabidopsis suspensor achieves its maximum length with a minimum number of cells by having a rod-shaped structure built by a single cell file. Although several mutants with distorted or shorter suspensors have been described in Arabidopsis, little is known about what impact suspensor length has on embryo development (Schwartz et al., 1994;Vernon and Meinke, 1994;Lukowitz et al., 2004;Breuninger et al., 2008;Bayer et al., 2009;Jeong et al., 2011b).As in all plant cells, the size and shape of suspensor cells is primarily determined by the elasticity of the cell wall. While rigid cellulose microfibrils determine the direction of cell expansion, it is the p...
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