A multigenotype maize silk expression atlas reveals how exposure-related stresses are mitigated following emergence from husk leaves

Authors: MCNINCH, COLTON - Iowa State University; CHEN, KETING - Iowa State University; DENNISON, TESIA - Iowa State University; Lopez, Miriam; YANDEAU-NELSON, MARNA - Iowa State University; Lauter, Nicholas

Submitted to: The Plant Genome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/5/2020
Publication Date: 10/14/2020
Citation: McNinch, C., Chen, K., Dennison, T.S., Lopez, M.D., Yandeau-Nelson, M.D., Lauter, N.C. 2020. A multigenotype maize silk expression atlas reveals how exposure-related stresses are mitigated following emergence from husk leaves. The Plant Genome. 13(3). Article e20040. https://doi.org/10.1002/tpg2.20040.
DOI: https://doi.org/10.1002/tpg2.20040

Interpretive Summary: Each year, growers across the globe collectively produce approximately one million corn kernels per human on the planet. As stigmatic organs, maize silks are required for each of the ~7 quadrillion pollen reception events associated with this grain production, yet the biological complexities of silk form and function are not yet well understood. When compared to stigmata across the ~300,000 species of flowering plants, corn silks are inordinately large, a requirement imposed by the protective husk leaves that fully encase an ear of corn. To protrude beyond the encasement to receive pollen, silks elongate at rates up to 4 cm per day and reach lengths of 50cm. Once emerged, they find themselves in a harsh aerial environment where they must simultaneously defend against abiotic and biotic stresses while remaining nourished and hydrated. Because silks inhabit these divergent environments the existence of functionally critical gene expression variation is expected to be readily discernible. To discover genetic and environmental variation in spatio-temporal gene expression, B73 and Mo17 silks for this investigation were sampled at three days following emergence from husk-leaves. Both the encased and emerged fractions were sub-sampled along a proximal-distal gradient, permitting investigation of interesting and largely unaddressed areas of silk biology. Analysis of functions for responsive genes revealed important roles of gene expression in silk development, metabolism, physiology and abiotic- and biotic-defense. The data sets produced by this study are expected to be widely used in agricultural research focusing on both stress response and plant reproductive biology.

Technical Abstract: Stigmatic tissue is required for sexual reproductive success in flowering plants. Silks are the extraordinarily long stigmatic organs of maize that emerge from a well-protected husk-encasement into harsh external environments for pollen reception. Understanding how gene expression changes along their length and between encased and emerged states offers a model for how silks develop and respond to their environment. Transcriptomic analysis of contiguous silk sections of inbred lines B73 and Mo17 identified both unique and conserved expression changes that are most dramatic at the point of emergence. Genes differentially expressed between husk-encased and emerged silks are strongly enriched for gene ontology terms associated with abiotic and biotic stress responses, hormone signaling, defense metabolism and cell-cell communication. Generally, but with interesting exceptions, these genes are up-regulated upon emergence. Indeed, meta-analysis together with seven transcriptomic studies of various seedling treatments indicates that emergence and drought stresses are most similar. Finally, a genome correlation network analysis identified 26 expression clusters, revealing additional complexities. For example, genotypically divergent expression clusters of genes encoding proteins involved in photosynthetic reactions suggests genetic variation for primary physiological processes in silks. This silk transcriptomic dataset provides a valuable resource for future investigations of stigmatic biology and pollen receptivity.