Expansin helps maize to keep the right timing: inducible expression of an Expansin gene mitigates drought effects on grain yields

Sexual reproduction is a question of timing. In other words, mating requires meeting, which means being in the right place at the right time. Maize is a monoecious outcrossing species that is also capable of self-pollination and requires only a light breeze to deliver pollen from male inflorescences (tassels) at the top of the stalks to female inflorescences (ears) located in the middle of the same stalk or nearby plants. All that is left is the timing, which in maize is known as the anthesis-silking interval (ASI). In optimal conditions, ASI is short and anthesis, when mature pollen grains are released from the tassel, is synchronized with silking, the emergence from the ear of elongated stigmas (known as silks) that are ready to receive pollen and begin the fertilization process. However, water scarcity at flowering increases the ASI, leading to asynchronous development of tassel and ear that ultimately impairs pollination and causes significant yield losses (Bolaños and Edmeades, 1996). In this issue, Liu et al. (2021) investigated the effect of water limitation on maize reproductive growth and found ASI asynchronism to be associated with defects in ear development rather than tassel development. Water stress did not cause morphological alterations of reproductive organs but delayed ear development as well as reduced silk growth. Eventually, 1-week retardation in the date of silking led to significantly reduced seed production. To decipher the molecular mechanisms underlying stress-induced ASI asynchronism, the authors developed a transcriptome atlas of maize ears collected at different developmental stages from plants grown under increasing water limitation. Gene ontology analysis revealed enrichment of terms related to DNA replication and transcription processes in the transcriptome of 5- to 10-mm ears, and terms related to cell growth and expansion (e.g. cell wall biogenesis and vacuoles) in the transcriptome of 50-mm ears. Interestingly, developmental processes had a greater influence on the ear transcriptome than drought. For example, relative transcript levels of known MADS-box genes involved in the specification of floral organ identity gradually increased during ear development but were unaffected by water limitation. Nevertheless, among those genes highly transcribed in 50-mm ears, drought altered the expression of categories related to cell expansion and floral organ enlargement—including components of the auxin signaling pathway, photosynthesis-related processes, and cell wall functioning. In particular, drought-mediated downregulation of genes encoding Expansins (EXPs) and xyloglucan endotransglycosylases (XETs), which modify cell wall extensibility, could be related to delayed growth and reduced extension of silks in response to water stress. Effect of drought on ear development and silk elongation. In developing ears, high expression of factors involved in cell expansion (EXPs and XETs) is correlated with silk elongation under well-watered conditions (left) but their downregulation in response to water stress is associated with reduced silk extension (right). Figure credit: M. Osnato; adapted from Liu et al. (2021); Figure 6. By exploring the natural genetic variation of a population of 228 maize accessions (Liu et al., 2020), the authors discovered an association between phenotypic variation in ASI and polymorphisms at an EXP locus, likely affecting gene expression. In particular, accessions with higher ZmEXPA4 expression ratio between water stress and well-watered conditions had less ASI asynchronism. Similar results were also obtained in transgenic plants with altered accumulation of ZmEXPA4. Indeed, specific activation of this gene in developing ears driven by a drought-inducible promoter significantly reduced ASI asynchronism under water deficit without penalizing yield in all conditions tested. The exploitation of natural diversity and genetic engineering represent alternative strategies to obtain novel varieties able to maintain high crop yield potential in a global change scenario. Notably, the use of inducible systems to drive the expression of interesting genes in specific tissues or developmental stages could be a precise biotechnological tool to enhance drought resilience without affecting plant production, as suggested by Gupta et al. (2021). Liu et al. show that EXP genes may represent good candidates for improving drought tolerance and helping maize get its timing right.