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Identification of source-sink tissues in the leaf of Chinese cabbage (Brassica rapa ssp. pekinensis) by carbohydrate content and transcriptomic analysis

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Abstract

Background

A leaf of Chinese cabbage (Brassica rapa ssp. pekinensis) is composed of a photosynthetic blade and a non-photosynthetic large midrib; thus each leaf contains both source and sink tissues. This structure suggests that, unlike in other plants, source-sink metabolism is present in a single leaf of Chinese cabbage.

Objective

This study was designed to identify the transport route of photosynthetic carbon and to determine whether both source and sink tissues were present in a leaf.

Methods

Plant samples were collected diurnally. Their carbohydrate contents were measured, and a genome-wide transcriptome analysis was performed using the Br300K microarray. Expression profiles of selected genes were validated using qRT-PCR analysis.

Results

The presence of two contrasting tissues (blade as source and midrib as sink) in a leaf was demonstrated by (1) diurnal distribution patterns of starch and sucrose content; (2) Gene Ontology (GO) enrichment analysis of microarray data; (3) expression profiles of photosynthetic and sucrose biosynthetic genes; and (4) expression patterns of a variety of sugar transporter genes.

Conclusion

Source and sink tissues were both present in Chinese cabbage leaves, but the midrib functioned as a sink tissue as well as a site exporting to roots and other sink tissues. Function of most genes discriminating between source and sink tissue appeared to be regulated largely at the post-transcriptional level, not at the transcriptional level.

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Abbreviations

ACT2:

Actin 2

ADG1:

ADP glucose pyrophosphorylase small subunit 1

AKIN10:

Arabidopsis SNF1 kinase homolog 10

AKIN11:

Arabidopsis SNF1 kinase homolog 11; SnRK1.1

AMY3:

Alpha-amylase-like 3

BAM6/BMY5:

Beta-amylase 6/beta-amylase 5

CCA1:

Circadian clock-associated 1

CHLSYN:

Chlorophyll synthase

CINV1:

Cytosolic invertase 1

CpFBPase:

Chloroplastic fructose-1,6-bisphosphatase

CWINV1:

Cell wall invertase 1

CytFBPase:

Cytosolic fructose-1,6-bisphosphatase

DBE1:

Debranching enzyme 1

EMB2729:

Alpha-amylase family protein

ERD6:

Early response to dehydration 6

ERD6-Like 7:

Major facilitator superfamily protein

GLT1:

Glucose transporter 1

HKL1:

Hexokinase-like 1

HKL3:

Hexokinase-like 3

HXK1:

Glucose insensitive 2

HXK2:

Hexokinase 2

HXK3:

Hexokinase 3

HXK4:

Hexokinase 4

INT1:

Inositol transporter 1

INT4:

Inositol transporter 4

IPMI:

Invertase/pectin methylesterase inhibitor family protein

ISA1:

Isoamylase 1/alpha-amylase

ISA3:

Isoamylase 3

LDA/PU1:

Limit dextrinase/Pullulanase 1

LHY:

Late elongated hypocotyl

LSH1:

Light-dependent short hypocotyl 1

OCT4:

Organic cation/carnitine transporter 4

PETE1:

Plastocyanin

PHT2:

Phosphate transporter 2

PHT6:

Phosphate transporter 6

PMT5/PLT5:

Polyol/monosaccharide transporter 5

PORB:

Protochlorophyllide oxidoreductase B

PORC:

Protochlorophyllide oxidoreductase C

PSBA:

Photosystem II protein D1

RUBISCO:

Ribulose 1,5-bisphosphate carboxylase/oxygenase

RBCS-1A:

RuBisCO small subunit 1A

RBCS-2B:

RuBisCO small subunit 2B

RCA:

RUBISCO ACTIVASE

SBE2.1:

Starch branching enzyme 2.1

SBE2.2:

Starch branching enzyme 2.2

SNF:

Sucrose non-fermenting

SnRK1:

SNF-related kinase 1

SPP1:

Sucrose-phosphatase 1

SPP3:

Sucrose-phosphatase 3

SPS:

Sucrose phosphate synthase

SS3:

Starch synthase 3

STP1:

Sugar transporter 1

STP13:

Sugar transporter protein 13

STP4:

Sugar transporter 4

STP6:

Sugar transporter 6

STP7:

Sugar transporter 7

SUC1:

Sugar-proton symporter 1

SUC2:

Sugar-proton symporter 2

SUC3/SUT2:

Sucrose transporter 3

SUC4/SUT4:

Sucrose transporter 4

SUC7:

Sucrose-proton symporter 7

SUS1:

Sucrose synthase 1

SUS3:

UDP-glycosyltransferase/sucrose synthase 3

SUS6:

UDP-glycosyltransferase/sucrose synthase 6

TMT1:

Tonoplast monosaccharide transporter 1

TMT2:

Tonoplast monosaccharide transporter 2

TOC1:

Timing of CAB expression

TOR:

Target of rapamycin

UTR3:

UDP-galactose transporter 3

UTR6:

UDP-galactose transporter 6

VAC-INV:

Vacuolar invertase

VGT1:

Vacuolar glucose transporter 1

3008:

Pollen Ole e 1 allergen and extensin family protein

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Acknowledgements

This work was supported by a grant from the Research Fund of Chungnam National University (CNU), Daejeon, Korea, to Yoonkang Hur (2018-1201-01).

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Author notes

  1. Jeongyeo Lee and Xiangshu Dong equal contributors.

Authors and Affiliations

  1. Department of Biological Sciences, Chungnam National University, Daejeon, 34134, Republic of Korea

    Jeongyeo Lee, Xiangshu Dong, Kwan Choi, Hayong Song, Hankuil Yi & Yoonkang Hur

  2. Korea Research Institute of Bioscience and Biotechnology, Daejeon, 34141, Republic of Korea

    Jeongyeo Lee

  3. School of Agriculture, Yunnam University, Kunming, 650091, China

    Xiangshu Dong

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  1. Jeongyeo Lee
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  2. Xiangshu Dong
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Correspondence to Yoonkang Hur.

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Lee, J., Dong, X., Choi, K. et al. Identification of source-sink tissues in the leaf of Chinese cabbage (Brassica rapa ssp. pekinensis) by carbohydrate content and transcriptomic analysis. Genes Genom 42, 13–24 (2020). https://doi.org/10.1007/s13258-019-00873-z

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