High-resolution spatiotemporal transcriptome mapping of tomato fruit development and ripening

Authors: SHINOZAKI, YOSHITO - Cornell University; NICOLAS, PHILIPPE - Boyce Thompson Institute; FERNANDEZ-POZO, NOE - Boyce Thompson Institute; EVANICH, DANIEL - Boyce Thompson Institute; SHI, YANNA - Boyce Thompson Institute; Thannhauser, Theodore - Ted; MUELLER, LUKAS - Cornell University; FEI, ZHANGJUN - Boyce Thompson Institute; Giovannoni, James; ROSE, JOCELYN - Cornell University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/22/2017
Publication Date: 1/25/2018
Citation: Shinozaki, Y., Nicolas, P., Fernandez-Pozo, N., Evanich, D., Shi, Y., Thannhauser, T.W., Mueller, L., Fei, Z., Giovannoni, J.J., Rose, J. 2018. High-resolution spatiotemporal transcriptome mapping of tomato fruit development and ripening. Nature Communications. 9:364.

Interpretive Summary: The fleshy fruits of angiosperms have evolved elaborate physiological and biochemical processes to promote animal attraction, consumption, and seed dispersal. Tomato (Solanum lycopersicum) has emerged as the principal model to study fleshy fruit development and ripening, and to investigate the molecular bases of commercially important traits, including fruit set, size, texture, color, flavor, aroma, and nutritional quality which support an industry with an estimated annual market value of >$55 billion. Such targeted studies are supported by large-scale “omics”-based analyses of tomato fruit, including transcriptome, proteome, metabolome, and epigenome profiling initiatives. We present here a comprehensive tomato fruit transcriptome atlas, incorporating global gene expression and co-expression data at a cell- or tissue-type level of resolution across the gamut of developmental stages, spanning early fruit growth and ripening. In addition, we take into account the fact that tomato fruit ripen along a latitudinal gradient, starting at the stylar, or blossom, end and spreading basipetally to the stem end, and examine transcriptional dynamics along this axis. We use these data sets to characterize the distribution and timing of gene regulatory and structural networks along spatial and developmental gradients, including functional evaluation of specific hormonal and epigenetic control points, thereby elucidating diverse aspects of fleshy fruit biology and quality traits that are typically indistinguishable in unseparated cells or tissues.

Technical Abstract: Tomato (Solanum lycopersicum) is an established model for studying fruit biology; however, most studies of tomato fruit growth and ripening are based on homogenized pericarp, and do not consider the internal tissues, or the expression signatures of individual cell and tissue types. We present a spatiotemporally resolved transcriptome analysis of tomato fruit ontogeny, using laser microdissection (LM) or hand dissection coupled with RNA-Seq analysis. Regulatory and structural gene networks, including families of transcription factors and hormone synthesis and signaling pathways, are defined across tissue and developmental spectra. The ripening program is revealed as comprising gradients of gene expression, initiating in internal tissues then radiating outward, and basipetally along a latitudinal axis. We also identify spatial variations in the patterns of epigenetic control superimposed on ripening gradients. Functional studies elucidate previously masked regulatory phenomena and relationships, including those associated with fruit quality traits, such as texture, color, aroma, and metabolite profiles.