Many plants dramatically elongate their stems during flowering, yet how this response is coordinated with the reproductive phase is unclear. We demonstrate that microRNA (miRNA) control of APETALA2 (AP2) is required for rapid, complete elongation of stem internodes in barley, especially of the final ‘peduncle’ internode directly underneath the inflorescence. Disrupted miR172 targeting of AP2 in the Zeo1.b barley mutant caused lower mitotic activity, delayed growth dynamics and premature lignification in the peduncle leading to fewer and shorter cells. Stage- and tissue-specific comparative transcriptomics between Zeo1.b and its parent cultivar showed reduced expression of proliferation-associated genes, ectopic expression of maturation-related genes and persistent, elevated expression of genes associated with jasmonate and stress responses. We further show that applying methyl jasmonate (MeJA) phenocopied the stem elongation of Zeo1.b, and that Zeo1.b itself was hypersensitive to inhibition by MeJA but less responsive to promotion by gibberellin. Taken together, we propose that miR172-mediated restriction of AP2 may modulate the jasmonate pathway to facilitate gibberellin-promoted stem growth during flowering.

The plant hormone auxin regulates a wide variety of transcriptional responses depending on the cell type, environment and species. How this diversity is achieved may be related to the specific complement of auxin-signalling components in each cell. The levels of activators (class-A AUXIN RESPONSE FACTORS) and repressors (class-B ARFs) are particularly important. Tight regulation of ARF protein levels is probably key in determining this balance. Through comparative analysis of novel, dominant mutants in maize and the moss Physcomitrium patens, we have discovered a ~500-million-year-old mechanism of class-B ARF protein-level regulation mediated by proteasome degradation, important in determining cell fate decisions across land plants. Thus, our results add a key piece to the puzzle of how auxin regulates plant development.

Faced with terrestrial threats, land plants seal their aerial surfaces with a lipid-rich cuticle. To breathe, plants interrupt their cuticles with adjustable epidermal pores, called stomata, that regulate gas exchange, and develop other specialised epidermal cells such as defensive hairs. Mechanisms coordinating epidermal features remain poorly understood. Addressing this, we studied two loci whose allelic variation causes both cuticular wax-deficiency and misarranged stomata in barley, identifying the underlying genes,Cer-g/HvYDA1, encoding a YODA-like (YDA) MAPKKK, andCer-s/HvBRX-Solo, encoding a single BREVIS-RADIX (BRX) domain protein. Both genes control cuticular integrity, the spacing and identity of epidermal cells, and barley’s distinctive epicuticular wax blooms, as well as stomatal patterning in elevated CO₂conditions. Genetic analyses revealed epistatic and modifying relationships betweenHvYDA1andHvBRX-Solo, intimating that their products participate in interacting pathway(s) linking epidermal patterning with cuticular properties in barley. This may represent a mechanism for coordinating multiple adaptive features of the land plant epidermis in a cultivated cereal.

All land plants seal their above ground body parts with a lipid-rich hydrophobic barrier called the cuticle to protect themselves from dehydration and other terrestrial threats. Mutational studies in several model species have identified multiple loci regulating cuticular metabolism and development. Of particular importance are the eceriferum (cer) mutants characterized by a loss of cuticular wax. Some barley cer mutants, including cer-x, show defects in the distinctive β-diketone-enriched wax bloom on reproductive stage leaf sheaths, stems, and spikes. We exploited extensive allelic populations, near-isogenic lines, and powerful genotyping platforms to identify variation in the HvWAX INDUCER1 (HvWIN1) gene, encoding a SHINE transcription factor, as underlying cer-x. Comparing the cer-x allelic glossy sheath4.l Bowman Near Isogenic Line BW407 to cv. Bowman revealed an increased cuticular permeability in tissues showing reduced accumulation of β-diketones and altered cuticular metabolic gene expression in BW407. Analyses across the barley pangenome and hundreds of exome-capture datasets revealed high sequence conservation of HvWIN1 and two non-synonymous variants exclusive to the cultivated germplasm. Taken together, we suggest that variation in HvWIN1 controls multiple cuticular features in barley.

The cuticle covering aerial organs of land plants is well known to protect against desiccation. Cuticles also play diverse and specialized functions, including organ separation, depending on plant and tissue. Barley shows a distinctive cuticular wax bloom enriched in β-diketones on leaf sheaths, stem nodes and internodes and inflorescences. Barley also develops a sticky surface on the outer pericarp layer of its grain fruit leading to strongly adhered hulls, ‘covered grain’, important for embryo protection and seed dispersal. While the transcription factor-encoding gene HvNUDUM (HvNUD) appears essential for adherent hulls, little is understood about how the pericarp cuticle changes during adhesion or whether changes in pericarp cuticles contribute to another phenotype where hulls partially shed, called ‘skinning’. To that end, we screened barley lines for hull adhesion defects, focussing on the Eceriferum (= waxless, cer) mutants. Here, we show that the cer-xd allele causes defective wax blooms and compromised hull adhesion, and results from a mutation removing the last 10 amino acids of the GDS(L) [Gly, Asp, Ser, (Leu)]-motif esterase/lipase HvGDSL1. We used severe and moderate HvGDSL1 alleles to show that complete HvGDSL1 function is essential for leaf blade cuticular integrity, wax bloom deposition over inflorescences and leaf sheaths and pericarp cuticular ridge formation. Expression data suggest that HvGDSL1 may regulate hull adhesion independently of HvNUD. We found high conservation of HvGDSL1 among barley germplasm, so variation in HvGDSL1 unlikely leads to grain skinning in cultivated barley. Taken together, we reveal a single locus which controls adaptive cuticular properties across different organs in barley.

Summary: The grass leaf plays a critical role in global food security, generating the carbon stores in cereal grains, which provide > 50% of global calories. As the global population grows, there is an urgent need to increase food production using fewer resources and to develop more resilient agricultural systems to withstand variable climate conditions and rising socio‐economic and environmental costs. Precision engineering of cereal crops, tailored to diverse environmental conditions and agronomic practices, is a vital strategy for achieving food security. Given the fundamental importance of the leaf in driving cereal productivity, it is an ideal engineering target. Leaf development occurs over large temporal and spatial scales and is environmentally regulated, posing significant challenges for predictive engineering approaches and limiting the feasibility of a one‐size‐fits‐all approach. In this review, we synthesise current understanding of cereal leaf development and identify critical developmental biology questions that must be resolved to facilitate the truly programmable plants of the future.