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

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

doi:10.1038/s41467-017-02782-9

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.

Highlights

Tomato (Solanum lycopersicum) is an established model for studying fruit biology; 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
Similar numbers were expressed at individual stages, but in general, more were detected during fruit expansion (Supplementary Fig. 4)
Among the pericarp cell types, we found that several genes encoding key enzymes involved in starch biosynthesis, including ADP-glucose pyrophosphorylase (AGPase) and starch-branching enzyme, showed abundant expression in the parenchyma (Fig. 4a)

Summary

Introduction

Tomato (Solanum lycopersicum) is an established model for studying fruit biology; 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. 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[3,4], which support an industry with an estimated annual market value of > $55 billion[5]. 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[14], 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

Methods

Results

Conclusion