Polar auxin transport together with AINTEGUMENTA and REVOLUTA coordinate early Arabidopsis gynoecium development

In flowering plants the gynoecium is the female reproductive structure and the site of oogenesis, fertilization, and maturation of the embryo and the seed. Proper development of the gynoecium requires that the early gynoecial primordium be partitioned into distinct spatial domains with divergent fates. Regulated transport of the phytohormone auxin previously has been shown to play a role in the patterning of spatial domains along the apical-basal axis of the gynoecium. Here we establish a role for auxin transport in patterning along the medio-lateral axis of the gynoecial ovary. We demonstrate that auxin transport is required for the development of the medial ovary domain that contains the carpel margin meristem, a vital female reproductive structure. Disruptions in auxin transport enhance the medial domain defects observed in aintegumenta and revoluta mutant genotypes. AINTEGUMENTA and REVOLUTA are likely to function in parallel and partially overlapping pathways required for medial domain development. Our data indicate that different ovary domains are differentially sensitive to the reduction of polar auxin transport and the loss of AINTEGUMENTA and REVOLUTA activity. We suggest that an auxin-mediated positional cue is important for the differential specification of the medial and lateral ovary domains.     

Homology,limbs, and genitalia

SUMMARY Similarities in genetic control between the main body axis and its appendages have been generally explained in terms of genetic co-option. In particular, arthropod and vertebrate appendages have been explained to invoke a common ancestor already provided with patterned body outgrowths or independent recruitment in limb patterning of genes or genetic cassettes originally used for purposes other than axis patterning. An alternative explanation is that body appendages, including genitalia, are evolutionarily divergent duplicates (paramorphs) of the main body axis. However, are all metazoan limbs and genitalia homologous? The concept of body appendages as paramorphs of the main body axis eliminates the requirement for the last common ancestor of limb-bearing animals to have been provided with limbs. Moreover, the possibility for an animal to express complex organs ectopically demonstrates that positional and special homology may be ontogenetically and evolutionarily uncoupled. To assess the homology of animal genitalia, we need to take into account three different sets of mechanisms, all contributing to their positional and/or special homology and respectively involved (1) in the patterning of the main body axis, (2) in axis duplication, followed by limb patterning mechanisms diverging away from those still patterning the main body axis (axis paramorphism), and (3) in controlling the specification of sexual/genital features, which often, but not necessarily, come into play by modifying already developed and patterned body appendages. This analysis demonstrates that a combinatorial approach to homology helps disentangling phylogenetic and ontogenetic layers of homology.     

Auxin Influx Carriers Control Vascular Patterning and Xylem Differentiation in Arabidopsis thaliana

Auxin is an essential hormone for plant growth and development. Auxin influx carriers AUX1/LAX transport auxin into the cell, while auxin efflux carriers PIN pump it out of the cell. It is well established that efflux carriers play an important role in the shoot vascular patterning, yet the contribution of influx carriers to the shoot vasculature remains unknown. Here, we combined theoretical and experimental approaches to decipher the role of auxin influx carriers in the patterning and differentiation of vascular tissues in the Arabidopsis inflorescence stem. Our theoretical analysis predicts that influx carriers facilitate periodic patterning and modulate the periodicity of auxin maxima. In agreement, we observed fewer and more spaced vascular bundles in quadruple mutants plants of the auxin influx carriers aux1lax1lax2lax3. Furthermore, we show AUX1/LAX carriers promote xylem differentiation in both the shoot and the root tissues. Influx carriers increase cytoplasmic auxin signaling, and thereby differentiation. In addition to this cytoplasmic role of auxin, our computational simulations propose a role for extracellular auxin as an inhibitor of xylem differentiation. Altogether, our study shows that auxin influx carriers AUX1/LAX regulate vascular patterning and differentiation in plants.     

AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis

In contrast to animals, little is known about pattern formation in plants. Physiological and genetic data suggest the involvement of the phytohormone auxin in this process. Here, we characterize a novel member of the PIN family of putative auxin efflux carriers, Arabidopsis PIN4, that is localized in developing and mature root meristems. Atpin4 mutants are defective in establishment and maintenance of endogenous auxin gradients, fail to canalize externally applied auxin, and display various patterning defects in both embryonic and seedling roots. We propose a role for AtPIN4 in generating a sink for auxin below the quiescent center of the root meristem that is essential for auxin distribution and patterning.     

Polarity and signalling in plant embryogenesis

The establishment of the apical-basal axis is a critical event in plant embryogenesis, evident from the earliest stages onwards. Polarity is evident in the embryo sac, egg cell, zygote, and embryo-suspensor complex. In the embryo-proper, two functionally distinct meristems form at each pole, through the localized expression of key genes. A number of mutants, notably of the model genetic organism Arabidopsis thaliana, have revealed new gene functions that are required for patterning of the apical-basal axis. There is now increasing evidence that two particular modes of signalling, via auxin and cell wall components, play important roles in co-ordinating the gene expression programmes that define determinative roles in the establishment of polarity.     

Auxin transport synchronizes the pattern of cell division in a tobacco cell line

The open morphogenesis of plants requires coordination of patterning by intercellular signals. The tobacco (Nicotiana tabacum cv Virginia Bright Italia) cell line VBI-0 provides a simple model system to study the role of intercellular communication in patterning. In this cell line, singular cells divide axially to produce linear cell files of distinct polarity. The trigger for this axial division is exogenous auxin. When frequency distributions of files are constructed over the number of cells per file during the exponential phase of the culture, even numbers are found to be frequent, whereas files consisting of uneven numbers of cells are rare. We can simulate these distributions with a mathematical model derived from nonlinear dynamics, which describes a chain of cell-division oscillators where elementary oscillators are coupled unidirectionally and where the number of oscillators is not conserved. The model predicts several nonintuitive properties of our experimental system. For instance, files consisting of six cells are more frequent than expected from a strictly binary division system. More centrally, the model predicts a polar transport of the coordinating signal. We therefore tested the patterns obtained after treatment with 1-N-naphthylphthalamic acid, an inhibitor of auxin efflux carriers. Using low concentrations of 1-N-naphthylphthalamic acid that leave cell division and axiality of division unaltered, we observe that the frequencies of files with even and uneven cell numbers are equalized. Our findings are discussed in the context of auxin transport as synchronizing signal in cell patterning.     

Wnt/beta-catenin signaling and body plan formation in mouse embryos

Wnt/beta-catenin signaling plays fundamental roles in body patterning in many invertebrate and vertebrate species, by acting as a key regulator of germ layer and body axis specification. This article focuses on the roles of Wnt/beta-catenin signaling in mouse early embryos, which exhibit a unique mode of development compared to non-mammalian vertebrates. Current experimental evidence suggests that Wnt/beta-catenin signaling is not essential for patterning embryos before implantation. However, Wnt/beta-catenin signaling regulates critical developmental events after implantation, namely the patterning of visceral endoderm, the induction of primitive streak, and the formation of anterior neural ectoderm. While Wnt/beta-catenin signaling regulates the body axis formation in both mouse and frog, the mode of its action is significantly diverged between these two vertebrate species.     

The case for morphogens in plants

Plants and animals have evolved as multicellular organisms independently of one another. This raises the intriguing question of whether plants and animals have developed similar or distinct patterning strategies to establish their body plans. Animals use concentration gradients of signals termed morphogens for tissue patterning, but whether they are also used by plants is unclear. Here we compare and contrast the plant hormone auxin with animal morphogens, and speculate as to whether plants have independently evolved similar mechanisms to regulate pattern formation.     

Modeling Auxin Transport and Plant Development

The plant hormone auxin plays a critical role in plant development. Central to its function is its distribution in plant tissues, which is, in turn, largely shaped by intercellular polar transport processes. Auxin transport relies on diffusive uptake as well as carrier-mediated transport via influx and efflux carriers. Mathematical models have been used to both refine our theoretical understanding of these processes and to test new hypotheses regarding the localization of efflux carriers to understand auxin patterning at the tissue level. Here we review models for auxin transport and how they have been applied to patterning processes, including the elaboration of plant vasculature and primordium positioning. Second, we investigate the possible role of auxin influx carriers such as AUX1 in patterning auxin in the shoot meristem. We find that AUX1 and its relatives are likely to play a crucial role in maintaining high auxin levels in the meristem epidermis. We also show that auxin influx carriers may play an important role in stabilizing auxin distribution patterns generated by auxin-gradient type models for phyllotaxis.     

Vascular patterning: more than just auxin?

The plant hormone auxin has long been known to play a pivotal role in vascular patterning and differentiation. But auxin is not the whole story: recent genetic analyses have identified additional factors required for vascular patterning, one of them involving sterols.