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

Yoshihito Shinozaki, Philippe Nicolas, Noe Fernandez-Pozo, Qiyue Ma, Daniel J. Evanich, Yanna Shi, Yimin Xu, Yi Zheng, Stephen I. Snyder, Laetitia B. B. Martin, Eliel Ruiz-May, Theodore W. Thannhauser, Kunsong Chen, David S. Domozych, Carmen Catalá, Zhangjun Fei, Lukas A. Mueller, James J. Giovannoni, Jocelyn K. C. Rose

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.