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

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...

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Published inThe 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
LanguageEnglish
Published England Blackwell Publishing Ltd 01.12.2018
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RNA
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Abstract 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.
AbstractList 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 14 C 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. 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.
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.
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 14 C 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.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 14 C 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.
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.
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.
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 C 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.
Author Nie, Jing
Shan, Nan
Sui, Xiaolei
Zheng, Yi
Scanlon, Michael J.
Zhang, Cankui
Li, Xin
Ma, Si
Fei, Zhangjun
Turgeon, Robert
Zhang, Zhenxian
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30194881$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2018 The Authors. published by John Wiley & Sons Ltd and Society for Experimental Biology.
2018 The Authors. The Plant Journal published by John Wiley & Sons Ltd and Society for Experimental Biology.
Copyright © 2018 John Wiley & Sons Ltd and the Society for Experimental Biology
Copyright_xml – notice: 2018 The Authors. published by John Wiley & Sons Ltd and Society for Experimental Biology.
– notice: 2018 The Authors. The Plant Journal published by John Wiley & Sons Ltd and Society for Experimental Biology.
– notice: Copyright © 2018 John Wiley & Sons Ltd and the Society for Experimental Biology
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Issue 5
Keywords RNA sequencing
internal phloem
cucumber (Cucumis sativus L.) fruit
vascular bundle
defense response
external phloem
transport
laser capture microdissection
Language English
License Attribution
2018 The Authors. The Plant Journal published by John Wiley & Sons Ltd and Society for Experimental Biology.
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  doi: 10.1111/j.1365-3040.2011.02380.x
– ident: e_1_2_8_26_1
  doi: 10.1111/pce.13053
SSID ssj0017364
Score 2.4341488
Snippet 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...
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...
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SubjectTerms 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
Title Transcriptomic and functional analysis of cucumber (Cucumis sativus L.) fruit phloem during early development
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Ftpj.14084
https://www.ncbi.nlm.nih.gov/pubmed/30194881
https://www.proquest.com/docview/2137392679
https://www.proquest.com/docview/2101276246
https://www.proquest.com/docview/2189519427
Volume 96
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