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Root transcriptome analysis on the grape genotypes with contrast translocation pattern of excess manganese from root to shoot

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Abstract

Aims

The root-to-shoot transport of manganese (Mn) exhibited intra-specific characters in different grape genotypes. The majority of Mn was stored in the roots of the grape cultivar Jinshou, while it was mainly transferred to the shoots in the cultivar Combier. The aims of the present study was to reveal the complex interplay of gene expression endowing grape a high tolerance to excess Mn and to explore the relation of the expression of Mn transporters with the contrast root-to-shoot translocation pattern of excess Mn in different grape cultivars.

Methods

The root transcriptome changes in both cultivars were analyzed by high-throughput sequencing and validated by quantitative RT-PCR.

Results and conclusion

Compared to Jinshou, Combier exhibited a markedly high transcripts level in the Mn transporter unigenes in the roots independent of the Mn treatment, accompanied by a higher expression level of genes encoding nicotianamine synthase, heavy metal-transporting ATPase, ZIP family member and IRT1-like proteins, which could facilitate Mn transport from the roots to the shoots in Combier. However, the expression level of genes involved in the subcellular vesicular transport pathway was much higher in Jinshou than in Combier, with a higher transcripts level of V-ATPase, vacuolar protein and the proteins for the synthesis of organic acid, such as the citrate cycle and glycolysis pathway. All of these changes allowed Mn to be easily chelated and compartmented to root cortical and epidermic cell vacuoles in Jinshou, accompanied with higher transcription and activity levels of stress-related enzymes, endowing Jinshou a high degree of tolerance to excess Mn. The grape transcriptome responses to Mn stress were also discussed.

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Abbreviations

Mn:

Manganese

DEG:

Differentially expressed gene

DGE:

Digital gene expression

TPM:

Number of transcripts per million clean tags

PCR:

Polymerase chain reaction

qRT-PCR:

Quantitative real time polymerase chain reaction

CAT:

Catalase

APX:

Ascorbate peroxidase

POD:

Guaiacol peroxidase

SOD:

Superoxide dismutase

CK:

The control

MDA:

Malondialdehyde

BTC:

Biological transfer coefficient

KEGG:

Kyoto Encyclopedia of Genes and Genomes

IRT:

Iron-regulated transporter

MT:

Metallothioneins

HMA:

Heavy metal-transporting P-type ATPase

NAS:

Nicotianamine synthase

MTP:

Metal tolerance protein

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Acknowledgments

This research was supported by the talent program of Southwestern University of Science and Technology (No. 13zx7116) as well as the foundation of Sichuan Engineering Center for Biomass Resource exploitation and modification (No. 12zxsk10), Youth foundation of science and technology in Sichuan (No. No.2014JQ0016) and Project of Innovation research team in Sichuan Education Administration (No. 13TD0023).

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Authors and Affiliations

  1. School of life science and engineering, Southwest University of Science and Technology, Mianyang, 621010, China

    Yinan Yao, Yongbin Ou & Xiuli Wu

  2. Key Laboratory of Biogeography and Bioresources, Xinjiang Institute of Ecology and Geography, Chinese Academy of Science, Urumqi, 830011, China

    Yinan Yao & Xinlong Xiao

  3. Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for Research and Development of Fine Chemicals of Guizhou University, Guizhou University, Guiyang, 550025, People’s Republic of China

    Gang Xu

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  1. Yinan Yao
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  2. Xinlong Xiao
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  3. Yongbin Ou
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  4. Xiuli Wu
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  5. Gang Xu
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Corresponding author

Correspondence to Gang Xu.

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Responsible Editor: Jian Feng Ma.

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Fig. S1

Saturation analysis of MPSS sequencing; a and b separately show the trend of sequence saturation of plant roots in the control and Mn-treated Combier; c and d separately show the trend of sequence saturation in the control and Mn treated Jinshou (GIF 56 kb)

(TIFF 27784 kb)

Fig. S2

Distribution of the total and distinct tags in the root libraries of two grapevine cultivars that were treated or not with Mn. a, c, e and g separately show the distribution of, respectively, the total tags in the CK of Combier, the Mn treatment of Combier, the CK of Jinshou, and the Mn treatment of Jinshou; b, d, f and h separately show the distribution of, respectively, the distinct total tags in the CK of Combier, the Mn treatment of Combier, the CK of Jinshou, and the Mn treatment of Jinshou (GIF 89 kb)

(TIFF 28228 kb)

Fig. S3

Comparison of transcript expression of different genes in the roots between two grapevine cultivars under control or Mn treatment conditions using the qRT-PCR and DGE techniques. The relative gene expression as measured by qRT-PCR was evaluated using the comparative cycle threshold method using Actin 1 as the reference gene. C-CK, control of Combier; C-Mn, Mn treatment of Combier; J-CK, control of Jinshou; J-Mn, Mn treatment of Jinshou. (GIF 120 kb)

(TIFF 27438 kb)

Fig. S4

Schematic diagram of the transcript changes of plant roots in the KEGG pathway between two grapevine cultivars under Mn-treated or control conditions (C-CK vs. J-CK; C-Mn vs. J-Mn). a, citrate cycle pathway (TCA cycle); b, snare interactions in vesicular transport. C-CK, control of Combier; C-Mn, Mn treatment of Combier; J-CK, control of Jinshou; J-Mn, Mn treatment of Jinshou. (XLS 142 kb)

Fig. S5

Schematic diagram of the transcript changes of plant roots in the KEGG pathway between two grapevine cultivars under Mn-treated or control conditions (C-CK vs. C-Mn; J-CK vs. J-Mn). a, glycolysis metabolism; b, photosynthesis; c, glycerophospholipid metabolism; d, N-glycan biosynthesis; e, glyoxylate and dicarboxylate metabolism; f, pyruvate metabolism; g, steroid biosynthesis; h, brassinosteroid biosynthesis. C-CK, control of Combier; C-Mn, Mn treatment of Combier; J-CK, control of Jinshou; J-Mn, Mn treatment of Jinshou. (XLS 466 kb)

Table S1

Primer sequences of the candidate genes fo qRT-PCR. (XLS 21 kb)

Table S2

Significantly enriched gene ontology (GO) terms in the Mn/CK root libraries of the two grape cultivars. (XLS 32 kb)

Table S3

Significant pathway enrichment analysis of the KEGG pathway in each pair of grape root libraries. (XLS 37 kb)

Table S4

DEGs for DNA repair in the roots between Combier and Jinshou. (XLS 20 kb)

Table S5

DEGs for auxin synthesis or oxidation in the roots between Combier and Jinshou. (XLS 22 kb)

Table S6

DEGs for stress-related protein in the roots between Combier and Jinshou. (XLS 62 kb)

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Yao, Y., Xiao, X., Ou, Y. et al. Root transcriptome analysis on the grape genotypes with contrast translocation pattern of excess manganese from root to shoot. Plant Soil 387, 49–67 (2015). https://doi.org/10.1007/s11104-014-2279-2

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