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TPST is involved in fructose regulation of primary root growth in Arabidopsis thaliana

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Abstract

Key message

TPST is involved in fructose signaling to regulate the root development and expression of genes in biological processes including auxin biosynthesis and accumulation in Arabidopsis.

Abstract

Sulfonation of proteins by tyrosine protein sulfotransferases (TPST) has been implicated in many important biological processes in eukaryotic organisms. Arabidopsis possesses a single TPST gene and its role in auxin homeostasis and root development has been reported. Here we show that the Arabidopsis tpst mutants are hypersensitive to fructose. In contrast to sucrose and glucose, fructose represses primary root growth of various ecotypes of Arabidopsis at low concentrations. RNA-seq analysis identified 636 differentially expressed genes (DEGs) in Col-0 seedlings in response to fructose verses glucose. GO and KEGG analyses of the DEGs revealed that fructose down-regulates genes involved in photosynthesis, glucosinolate biosynthesis and IAA biosynthesis, but up-regulates genes involved in the degradation of branched amino acids, sucrose starvation response, and dark response. The fructose responsive DEGs in the tpst mutant largely overlapped with that in Col-0, and most DEGs in tpst displayed larger changes than in Col-0. Interestingly, the fructose up-regulated DEGs includes genes encoding two AtTPST substrate proteins, Phytosulfokine 2 (PSK2) and Root Meristem Growth Factor 7 (RGF7). Synthesized peptides of PSK-α and RGF7 could restore the fructose hypersensitivity of tpst mutant plants. Furthermore, auxin distribution and accumulation at the root tip were affected by fructose and the tpst mutation. Our findings suggest that fructose serves as a signal to regulate the expression of genes involved in various biological processes including auxin biosynthesis and accumulation, and that modulation of auxin accumulation and distribution in roots by fructose might be partly mediated by the TPST substrate genes PSK-α and RGF7.

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Data availability

The sequencing data was deposited in NCBI Sequence Read Archive database as files of SRR9586777-9,586,780 (https://dataview.ncbi.nlm.nih.gov/object/PRJNA550232?reviewer=uqnklg8iipoaidlp7fasbu1shl) and files of SRR7644440-7,644,443 (https://dataview.ncbi.nlm.nih.gov/object/PRJNA484521?reviewer=kp1ejsmdcbkg4ckgidokhk9ugd).

Abbreviations

TPST:

Tyrosine protein sulfotransferases

RNA-seq:

RNA sequencing

DEGs:

Differentially expressed genes

GO:

Gene ontology

KEGG:

Kyoto encyclopedia of genes and genomes

PSK:

Phytosulfokine 2

RGF7:

Root meristem growth factor 7

mRGF7:

Mutated RGF7

ABA:

Abscisic acid

GIN:

Glucose insensitive

QTL:

Quantitative trait locus

FINS1:

Fructose insensitive1

CWIs:

Cell wall invertases

EMS:

Ethyle methyl sulfone

SUC2:

Sucrose transporter 2

MS:

Murashige and Skoog

IAA:

Indole-3-acetic acid

DIN:

Dark-induced proteins

COR15a:

Cold-regulated 15a (COR15a)

HOS2:

High expression of osmotically responsive genes 2

FLC:

Flowering locus C

CSP41B:

Chloroplast binding protein

ATM1:

Thioredoxin M-type 1

LHCB2:

Light-harvesting chlorophyll B-binding 2

ATPD:

ATP synthesis delta-subunit gene

PIF3:

Phytochrome interacting factor 3

CYP79F1:

Cytochrome P450 family 79 subfamily F polypeptide 1

TFs:

Transcription factors

COL9:

Constant-like 9

AIR1:

Auxin-induced in root cultures

RPKM:

Reads per kilobase of exon model per million mapped reads

cTPST-1:

Tpst-1 complementation line

cTPST-2:

Tpst-2 complementation line

WT:

Wild type

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Acknowledgements

We thank the genomics core facility at the Shanghai Center for Plant Stress Biology for whole genome sequencing and RNA sequencing, and thank the cell biology core facility at the Shanghai Center for Plant Stress Biology for confocal microscopy. We also thank Dr. Tongda Xu for providing the pDR5:GFP transgenic plant seeds. This research was supported by the Chinese Academy of Sciences (to J.-K.Z.), and the Scientific Research Fund of Hunan Provincial Education Department 15K059 and CX2017B388.

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Authors and Affiliations

  1. College of Bioscience and Biotechnology, Hunan Agricultural University, Changsha, 410128, China

    Yingli Zhong, Jiyong Xie & Suzhen Wen

  2. Shanghai Center for Plant Stress Biology, and Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 201602, China

    Yingli Zhong, Jiyong Xie, Suzhen Wen, Wenwu Wu, Li Tan, Mingguang Lei & Jian-kang Zhu

  3. Department of Chemistry and Biochemistry, Texas Tech University, Lubbock, TX, 79409, USA

    Huazhong Shi

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  1. Yingli Zhong
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YZ, Xie J, SW and LT conducted the experiments, WW performed the data analysis, ML provided materials and helped designing experiments, YX and HS drafted and revised the manuscript, J-KZ revised the manuscript.

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Zhong, Y., Xie, J., Wen, S. et al. TPST is involved in fructose regulation of primary root growth in Arabidopsis thaliana. Plant Mol Biol 103, 511–525 (2020). https://doi.org/10.1007/s11103-020-01006-x

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