Establishment of polarity in angiosperm lateral organs

In seed plants, lateral organs such as leaves and floral organs are formed from the flanks of apical meristems. Therefore, they have an inherent positional relationship: organ primordia have an adaxial side next to the meristem, and an abaxial one away from the meristem. Surgical and genetic studies suggest that a morphogenetic gradient, which originates in the meristem, converts the inherent polarity into a functional one. Once an adaxial-abaxial axis of polarity is established within organ primordia, it provides cues for proper lamina growth and asymmetrical development. Several key participants in this process have been identified, and analyses of these genes support and refine our views of axis formation in plants. The complex relationships between and within various members of these plant-specific gene families (class III HD-ZIPs, YABBYs and KANADIs) might account for a substantial part of the morphological variation in lateral organs of seed plants.     

Axis formation and polarity in plants.

We have recently gained insight into a number of mechanisms governing the formation of the major axes that define the embryonic and adult plant body plan. Phenotypic analysis and molecular characterization of mutants with aberrant morphogenesis has led to a better understanding of key processes including the generation of the shape of the apical embryo, the establishment and maintenance of the radial pattern of the root, and the placement of lateral organ primordia around the shoot apical meristem.     

Mechanisms and physiological role of polarity in plants

The concept of polarity was the starting point for the attempts of many investigators to understand the principles of differentiation, because the polar organization underlies specific three-dimensional structure of the organism and provides for the integrity and coordination of its functions. The polarity axes are established at the stage of zygote, extending to the developing embryo, and they ??vectorize?? subsequent plant growth and development. Polarization of cells and tissues is crucial for plant morphogenesis, because the emerging morphogenetic gradients provide the basis for differential genome activity at various stages of plant development. This review deals with the polarity phenomena and the mechanisms of symmetry axis formation at the level of cells and plant tissues. The roles of electrical gradients, Ca²⁺ ions, auxin, cytoskeleton, ROP-proteins, phosphoinositides, and microRNA in polarization of cells and tissues are considered.     

Establishment of anterior-posterior polarity in avian embryos.

In pre-streak chick embryos, the extraembryonic posterior marginal zone is able to induce an embryonic axis at an ectopic site without contributing cells to the induced primitive streak. This region expresses mesoderm-inducing factors that are capable of inducing an ectopic streak. Downstream of these events, chordin and bone morphogenetic protein acting within the central disc may play mutually opposing roles influencing streak formation. Although extraembryonic regions are important in establishing the embryonic axis, there does not appear to be an anterior region with head-inducing activity similar to that of the anterior visceral endoderm of the mammalian embryo.     

Cell polarity: Regulators and mechanisms in plants

Cell polarity plays an important role in a wide range of biological processes in plant growth and development.Cell polarity is manifested as the asymmetric distribution of molecules,for example,proteins and lipids,at the plasma membrane and inside of a cell.Here,we summarize a few polarized proteins that have been characterized in plants and we review recent advances towards understanding the molecular mechanism for them to polarize at the plasma membrane.Multiple mechanisms,including membrane trafficking,cytoskeletal activities,and protein phosphorylation,and so forth define the polarized plasma membrane domains.Recent discoveries suggest that the polar positioning of the proteo-lipid membrane domain may instruct the formation of polarity complexes in plants.In this review,we highlight the factors and regulators for their functions in establishing the membrane asymmetries in plant development.Furthermore,we discuss a few outstanding questions to be addressed to better understand the mechanisms by which cell polarity is regulated in plants.     

The role of JAGGED in shaping lateral organs

Position-dependent regulation of growth is important for shaping organs in multicellular organisms. We have characterized the role of JAGGED, a gene that encodes a protein with a single C(2)H(2) zinc-finger domain, in controlling the morphogenesis of lateral organs in Arabidopsis thaliana. Loss of JAGGED function causes organs to have serrated margins. In leaves, the blade region is most severely affected. In sepals, petals and stamens, the strongest defects are seen in the distal regions. By monitoring cell-cycle activity in developing petals with the expression of HISTONE 4, we show that JAGGED suppresses the premature differentiation of tissues, which is necessary for the formation of the distal region. The localization of defects overlaps with the expression domain of JAGGED, which is restricted to the growing regions of lateral organs. JAGGED expression is notably absent from the cryptic bract, the remnant of a leaf-like organ that subtends the flower in many species but does not normally develop in wild-type Arabidopsis. If misexpressed, JAGGED can induce the formation of bracts, suggesting that the exclusion of JAGGED from the cryptic bract is a cause of bractless flowers in Arabidopsis.     

Establishment of animal-vegetal polarity during maturation in ascidian oocytes

Mature ascidian oocytes are arrested in metaphase of meiosis I (Met I) and display a pronounced animal-vegetal polarity: a small meiotic spindle lies beneath the animal pole, and two adjacent cortical and subcortical domains respectively rich in cortical endoplasmic reticulum and postplasmic/PEM RNAs (cER/mRNA domain) and mitochondria (myoplasm domain) line the equatorial and vegetal regions. Symmetry-breaking events triggered by the fertilizing sperm remodel this primary animal-vegetal (a-v) axis to establish the embryonic (D-V, A-P) axes. To understand how this radial a-v polarity of eggs is established, we have analyzed the distribution of mitochondria, mRNAs, microtubules and chromosomes in pre-vitellogenic, vitellogenic and post-vitellogenic Germinal Vesicle (GV) stage oocytes and in spontaneously maturing oocytes of the ascidian Ciona intestinalis. We show that myoplasm and postplasmic/PEM RNAs move into the oocyte periphery at the end of oogenesis and that polarization along the a-v axis occurs after maturation in several steps which take 3-4 h to be completed. First, the Germinal Vesicle breaks down, and a meiotic spindle forms in the center of the oocyte. Second, the meiotic spindle moves in an apparently random direction towards the cortex. Third, when the microtubular spindle and chromosomes arrive and rotate in the cortex (defining the animal pole), the subcortical myoplasm domain and cortical postplasmic/PEM RNAs are excluded from the animal pole region, thus concentrating in the vegetal hemisphere. The actin cytoskeleton is required for migration of the spindle and subsequent polarization, whereas these events occur normally in the absence of microtubules. Our observations set the stage for understanding the mechanisms governing primary axis establishment and meiotic maturation in ascidians.     

Establishment of rostrocaudal polarity in tectal primordium: engrailed expression and subsequent tectal polarity.

In the E4 (embryonic day 4) chick tectal primordium, engrailed expression is strong at the caudal end and gradually weakens toward the rostral end. We used quail-chick chimeric tecta to investigate how the caudorostral gradient of engrailed expression is established and whether it is correlated with the subsequent rostrocaudal polarity of tectal development. To examine the positional value of the tectal primordium, we produced ectopic tecta in the diencephalon by transplanting a part of the mesencephalic alar plate heterotopically. In the ectopic tectum, the gradient of the engrailed expression reversed and the strength of the expression was dependent on the distance from the mes-diencephalon junction; the nearer the ectopic tectum was to the junction, the weaker the expression was. Consequently, the pattern of the engrailed expression in the host and ectopic tecta was nearly a mirror image, suggesting the existence of a repressive influence around the mes-diencephalon junction on the engrailed expression. We examined cytoarchitectonic development in the ectopic tecta, which normally proceeds in a gradient along the rostrocaudal axis; the rostral shows more advanced lamination than the caudal. In contrast, the caudal part of the ectopic tecta (near to the mes-diencephalon junction) showed more advanced lamination than the rostral. In both the host and ectopic tecta, advanced lamination was observed where the engrailed expression was repressed, and vice versa. Next we studied the correlation between engrailed expression and retinotectal projection from a view of plasticity and rigidity of rostrocaudal polarity in the tectum. We produced ectopic tecta by anisochronal transplantations between E3 host and E2 donor, and showed that there is little repressive influence at E3 around the mes-diencephalon junction. We then made chimeric double-rostral tectum (caudal half of it was replaced by rostral half of the donor tectum) or double-caudal tectum at E3. The transplants kept their original staining pattern in hosts. Consequently, the chimeric tecta showed wholly negative or positive staining of engrailed protein on the grafted side. In such tecta retinotectal projection pattern was disturbed as if the transplants retained their original position-specific characters. We propose from these heterotopic and anisochronal experiments that the engrailed expression can be a marker for subsequent rostrocaudal polarity in the tectum, both as regards cytoarchitectonic development and retinotectal projection.     

Establishment of cell polarity during early plant development

Cellular asymmetries have been proposed to play a role in plant embryogenesis. Genetic studies of Arabidopsis and other experimental approaches in several plant species have addressed the origins of cellular asymmetry in specific cases. Although zygote polarity, which precedes the formation of the apical—basal axis of the embryo, is normally aligned with that of the surrounding maternal tissue, isolated single somatic cells that give rise to embryos in culture appear to become polar in the absence of maternal factors. Gene expression patterns reveal the developmental consequences of cellular asymmetries occurring at later stages of embryogenesis. Genetic evidence suggests that these cellular asymmetries are established in response to as yet unidentified signals from adjacent cells.     

Cell polarity in plants: a PARspective on PINs

Plants have acquired the ability for organized multicellular development independent from animals. Because of this, they represent an independent example in nature for the development of coordinated, complex cell polarity from the simple polarity found in unicellular eukaryotes. Plants display a striking array of polarized cell types, with different axes of polarity being defined in one cell. The most investigated and best understood aspect of plant polarity is the apical-basal polarity of the PIN family of auxin efflux facilitators, which are of crucial importance for the organization of the entire plant body. Striking differences exist between the PAR-polarity modules known in animals and the ways PINs polarize plant cells. Nonetheless, a common regulatory logic probably applies to all polarizing eukaryotic cells, which includes self-reinforcing, positive feedback loops, intricate interactions between membrane-attached proteins, lipid signatures, and the targeting of transmembrane proteins to the correct domains of the plasma membrane.     

Establishment and expression of cellular polarity in fucoid zygotes.

Zygotes of fucoid algae have long been studied as a paradigm for cell polarity. Polarity is established early in the first cell cycle and is then expressed as localized growth and invariant cell division. The fertilized egg is a spherical cell and, by all accounts, bears little or no asymmetry. Polarity is acquired epigenetically a few hours later in the form of a rhizoid/thallus axis. The initial stage of polarization is axis selection, during which zygotes monitor environment gradients to determine the appropriate direction for rhizoid formation. In their natural setting in the intertidal zone, sunlight is probably the most important polarizing vector; rhizoids form away from the light. The mechanism by which zygotes perceive environmental gradients and transduce that information into an intracellular signal is unknown but may involve a phosphatidylinositol cycle. Once positional information has been recorded, the cytoplasm and membrane are reorganized in accordance with the vectorial information. The earliest detectable asymmetries in the polarizing zygote are localized secretion and generation of a transcellular electric current. Vesicle secretion and the inward limb of the current are localized at the presumptive rhizoid. The transcellular current may establish a cytoplasmic Ca2+ gradient constituting a morphogenetic field, but this remains controversial. Localized secretion and establishment of transcellular current are sensitive to treatment with cytochalasins, indicating that cytoplasmic reorganization is dependent on the actin cytoskeleton. The nascent axis at first is labile and susceptible to reorientation by subsequent environmental vectors but soon becomes irreversibly fixed in its orientation. Locking the axis in place requires both cell wall and F-actin and is postulated to involve an indirect transmembrane bridge linking cortical actin to cell wall. This bridge anchors relevant structures at the presumptive rhizoid and thereby stabilizes the axis. Approximately halfway through the first cell cycle, the latent polarity is expressed morphologically in the form of rhizoid growth. Elongation is by tip growth and does not appear to be fundamentally different from tip growth in other organisms. The zygote always divides perpendicular to the growth axis, and this is controlled by the microtubule cytoskeleton. Two microtubule-organizing centers on the nuclear envelope rotate such that they align with the growth axis. They then serve as spindle poles during mitosis. Cytokinesis bisects the axial spindle, resulting in a transverse crosswall. Although the chronology of cellular events associated with polarity is by now rather detailed, causal mechanisms remain obscure.     

Ups and downs of tissue and planar polarity in plants

The polar orientation of cells within a tissue is an intensively studied research area in animal cells. The term planar polarity refers to the common polar arrangement of cells within the plane of an epithelium. In plants, the subcellular analysis of tissue polarity has been limited by the lack of appropriate markers. Recently, research on plant tissue polarity has come of age. Advances are based on studies of Arabidopsis patterning, cell polarity and auxin transport mutants employing the coordinated, polar localization of auxin transporters and the planar polarity of root epidermal hairs as markers. These approaches have revealed auxin transport and response, vesicular trafficking, membrane sterol and cytoskeletal requirements of tissue polarity. This review summarizes recent progress in research on vascular tissue and planar epidermal polarity in the Arabidopsis root and compares it to findings on planar polarity in animals and cell polarity in yeast.