Opposite polarity programs regulate asymmetric subsidiary cell divisions in grasses.

Grass stomata recruit lateral subsidiary cells (SCs), which are key to the unique stomatal morphology and the efficient plant-atmosphere gas exchange in grasses. Subsidiary mother cells (SMCs) strongly polarise before an asymmetric division forms a SC. Yet apart from a proximal polarity module that includes PANGLOSS1 (PAN1) and guides nuclear migration, little is known regarding the developmental processes that form SCs. Here, we used comparative transcriptomics of developing wild-type and SC-less bdmute leaves in the genetic model grass Brachypodium distachyon to identify novel factors involved in SC formation. This approach revealed BdPOLAR, which forms a novel, distal polarity domain in SMCs that is opposite to the proximal PAN1 domain. Both polarity domains are required for the formative SC division yet exhibit various roles in guiding pre-mitotic nuclear migration and SMC division plane orientation, respectively. Nonetheless, the domains are linked as the proximal domain controls polarisation of the distal domain. In summary, we identified two opposing polarity domains that coordinate the SC division, a process crucial for grass stomatal physiology.

Generation of signaling specificity in Arabidopsis by spatially restricted buffering of ligand-receptor interactions.

Core signaling pathways function in multiple programs during multicellular development. The mechanisms that compartmentalize pathway function or confer process specificity, however, remain largely unknown. In Arabidopsis thaliana, ERECTA (ER) family receptors have major roles in many growth and cell fate decisions. The ER family acts with receptor TOO MANY MOUTHS (TMM) and several ligands of the EPIDERMAL PATTERNING FACTOR LIKE (EPFL) family, which play distinct yet overlapping roles in patterning of epidermal stomata. Here, our examination of EPFL genes EPFL6/CHALLAH (CHAL), EPFL5/CHALLAH-LIKE1, and EPFL4/CHALLAH-LIKE2 (CLL2) reveals that this family may mediate additional ER-dependent processes. chal cll2 mutants display growth phenotypes characteristic of er mutants, and genetic interactions are consistent with CHAL family molecules acting as ER family ligands. We propose that different classes of EPFL genes regulate different aspects of ER family function and introduce a TMM-based discriminatory mechanism that permits simultaneous, yet compartmentalized and distinct, function of the ER family receptors in growth and epidermal patterning.

Regional specification of stomatal production by the putative ligand CHALLAH.

The problem of modulating cell fate programs to create distinct patterns and distributions of specialized cell types in different tissues is common to complex multicellular organisms. Here, we describe the previously uncharacterized CHALLAH (CHAL) gene, which acts as a tissue-specific regulator of epidermal pattern in Arabidopsis thaliana. Arabidopsis plants produce stomata, the cellular valves required for gas exchange, in virtually all aerial organs, but stomatal density and distribution differ among organs and along organ axes. Such regional regulation is particularly evident in plants mutant for the putative receptor TOO MANY MOUTHS (TMM), which produce excess stomata in leaves but no stomata in stems. Mutations in CHAL suppress tmm phenotypes in a tissue-specific manner, restoring stomatal production in stems while minimally affecting leaves. CHAL is similar in sequence to the putative stomatal ligands EPF1 and EPF2 and, like the EPFs, can reduce or eliminate stomatal production when overexpressed. However, CHAL and the EPFs have different relationships to TMM and the ERECTA (ER) family receptors. We propose a model in which CHAL and the EPFs both act through ER family receptors to repress stomatal production, but are subject to opposite regulation by TMM. The existence of two such ligand classes provides an explanation for TMM dual functionality and tissue-specific phenotypes.

Asymmetric cell divisions: a view from plant development.

All complex multicellular organisms must solve the problem of generating diverse and appropriately patterned cell types. Asymmetric division, in which a single mother cell gives rise to daughters with distinct identities, is instrumental in the generation of cellular diversity and higher-level patterns. In animal systems, there exists considerable evidence for conserved mechanisms of polarization and asymmetric division. Here, we consider asymmetric cell divisions in plants, highlighting the unique aspects of plant cell biology and organismal development that constrain the process, but also emphasizing conceptual and mechanistic similarities with animal asymmetric divisions.