Transcriptomic and functional analysis of cucumber (Cucumis sativus L.) fruit phloem during early development

• Published in: The Plant journal : for cell and molecular biology Vol. 96; no. 5; pp. 982 - 996
• Main Authors: Sui, Xiaolei, Nie, Jing, Li, Xin, Scanlon, Michael J., Zhang, Cankui, Zheng, Yi, Ma, Si, Shan, Nan, Fei, Zhangjun, Turgeon, Robert, Zhang, Zhenxian
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.12.2018
• Subjects: Biosynthesis; carbon; Carbon 14; Computed tomography; cucumber (Cucumis sativus L.) fruit; cucumbers; Cucumis sativus; Cucumis sativus - growth & development; Cucumis sativus - metabolism; Cucumis sativus - ultrastructure; defense response; early development; Economic importance; external phloem; Fluorescence; Fluorescent dyes; Fluorescent indicators; Fruit - growth & development; Fruit - metabolism; Fruit - ultrastructure; Fruits; Functional analysis; Gene Expression Profiling; Gene sequencing; genes; internal phloem; Ion transport; laser capture microdissection; leaves; Metabolism; Metabolites; micro-computed tomography; microscopy; Microscopy, Confocal; Morphogenesis; Nitrogen compounds; Organs; peduncle; Phloem; Phloem - growth & development; Phloem - metabolism; Phloem - ultrastructure; Plant Stems - growth & development; Plant Stems - metabolism; Plant Stems - ultrastructure; Plant tissues; Protein transport; Proteins; radionuclides; Reproductive organs; Ribonucleic acid; RNA; RNA modification; RNA processing; RNA sequencing; RNA transport; secondary metabolites; sequence analysis; sieve tubes; Structure-function relationships; tracer techniques; Tracers; Transcription; transcription (genetics); transcriptomics; transport; Tubes; Unloading; vascular bundle; vascular bundles; Vascular tissue; X-Ray Microtomography; Xylem; Xylem - growth & development; Xylem - metabolism; Xylem - ultrastructure; RNA sequencing; internal phloem; cucumber (Cucumis sativus L.) fruit; vascular bundle; defense response; external phloem; transport; laser capture microdissection
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.14084

Summary The phloem of the Cucurbitaceae has long been a subject of interest due to its complex nature and the economic importance of the family. As in a limited number of other families, cucurbit phloem is bicollateral, i.e. with sieve tubes on both sides of the xylem. To date little is known about the specialized functions of the internal phloem (IP) and external phloem (EP). Here, a combination of microscopy, fluorescent dye transport analysis, micro‐computed tomography, laser capture microdissection and RNA‐sequencing (RNA‐Seq) were used to study the functions of IP and EP in the vascular bundles (VBs) of cucumber fruit. There is one type of VB in the peduncle, but four in the fruit: peripheral (PeVB), main (MVB), carpel (CVB) and placental (PlVB). The VBs are bicollateral, except for the CVB and PlVB. Phloem mobile tracers and 14C applied to leaves are transported primarily in the EP, and to a lesser extent in the IP. RNA‐Seq data indicate preferential gene transcription in the IP related to differentiation/development, hormone transport, RNA or protein modification/processing/transport, and nitrogen compound metabolism and transport. The EP preferentially expresses genes for stimulus/stress, defense, ion transport and secondary metabolite biosynthesis. The MVB phloem is preferentially involved in photoassimilate transport, unloading and long‐distance signaling, while the PeVB plays a more substantial role in morphogenesis and/or development and defense response. CVB and PlVB transcripts are biased toward development of reproductive organs. These findings provide an integrated view of the differentiated structure and function of the vascular tissue in cucumber fruit. Significance Statement The phloem of bicollateral vascular bundles (VBs) in the Cucurbitaceae has long been a subject of interest. However, little is known about the specialized functions of the internal (IP) and external phloem (EP) in these plants. This study provides a framework for understanding differentiated roles of IP and EP, and gene expression profiles of four interrelated VB systems in cucumber fruit.