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Characterization of Vv-miR156: Vv-SPL pairs involved in the modulation of grape berry development and ripening

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Abstract

SPL is a plant-specific transcription factor family. Many researchers reported that SPL members targeted by miR156s could play crucial roles in the modulation of plant growth and development. Although there are similar reports on grapes, till now little is known about grape berry development and ripening. To gain more insight into how grape miR156s (Vv-miR156s) modulated the above given processes of grape berries by mediating their target gene Vv-SPLs, here we identified the precise sequences of Vv-miR156s in ‘Giant Rose’ grape berries, predicted their potential targets, and revealed that the matching degree of various Vv-miR156: Vv-SPL pairs exhibited some discrepancy, implying the divergence of their interaction. Subsequently, we also discovered similar motifs such as ABRE, CGTCA and ERE, which are more specific to berry development and ripening, within the promoters of both Vv-MIR156s and Vv-SPLs. With berry development and ripening, meanwhile, Vv-miR156a, b/c/d, e and f/g/i exhibited an overall increasing expression trend, while their targets showed opposite trends at the corresponding stages. Additionally, exogenous ABA and NAA application promoted or curbed the expression of Vv-miR156s to some extent, before grape berry ripening stage. The cleavage products, sites and frequencies of Vv-miR156a, b/c/d, e, f/g/i and their respective targets (Vv-SPL2, 9, 10, 16) during grape berry development and ripening process were validated by our developed PPM-RACE and modified RLM-RACE together with qRT-PCR, which demonstrated that Vv-miR156s can be involved in the modulation of grape berry development and ripening process by mediating the expression of Vv-SPL2, 9, 10, 16. Our findings lay an important foundation for further recognizing their functions in grape berries, and enrich the knowledge of the regulatory mechanism of miRNA-mediated grape berry development and ripening.

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Abbreviations

SPL:

SQUAMOSA promoter-binding protein-like

SPB:

SQUAMOSA promoter-binding

PCR:

Polymerase chain reaction

qRT-PCR:

Quantitative real-time PCR

LMW:

Low-molecular-weight

HMW:

High-molecular-weight

RLM-RACE:

RNA ligase-mediated 5′ rapid amplification of cDNA ends

PPM-RACE:

Poly(A) polymerase-mediated 3′ rapid amplification of cDNA ends

nt:

Nucleotide

miRNA:

MicroRNA

CNR:

Colorless non-ripening

ABA:

Abscisic acid

NAA:

Naphthylacetic acid

MeJA:

Methyl jasmonate

BPP:

Berry pea-size period

BBT:

Beginning of berry touch

SHS:

Stone hardening stage

BTC:

Berry touch completion

BPR:

Beginning period of ripening

ECP:

Early colour-change period

CCP:

Colour-change period

BRP:

Berry ripening period

cv:

Cultivar

GA:

Gibberellin

SA:

Salicylic acid

GSP:

Gene-specific primers

mRNA:

Messenger RNA

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Acknowledgements

This research was supported by Project Funded via Special Program of China Postdoctoral Science Foundation (2014T70533), the Fundamental Research Funds for the Central Universities of China (KYZ201411), China Postdoctoral Science Foundation funded project (2013M531373), Jiangsu Postdoctoral Science Foundation Funded project (1301116C), and China Postdoctoral Science Foundation (2015M581811). In addition, we thank the Gene denovo company for the help in the bioinformatics analysis.

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Authors and Affiliations

  1. College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Mengjie Cui, Chen Wang, Wenying Zhang, Muhammad Salman Haider, Wei Tang & Jinggui Fang

  2. Department of Agriculture and Food Technology, Karakoram International University, Gilgit, 15100, Pakistan

    Tariq Pervaiz

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  1. Mengjie Cui
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  2. Chen Wang
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  3. Wenying Zhang
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  4. Tariq Pervaiz
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  5. Muhammad Salman Haider
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  6. Wei Tang
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  7. Jinggui Fang
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Contributions

CW conceived the study, and carried out the molecular mechanism analysis. MC and WZ conducted the expression analysis of miRNAs and their targets, and validated their cleavage roles. MC detected the accumulations of 3′-/5′-cleavage products of miRNAs on their targets at the diverse stages of grape berry development and ripening process. MH performed the promoter element analysis of miRNAs and their targets. MC and WT drew the tables and figures. CW drafted the manuscript. CW, TP, MH and JF revised the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Chen Wang or Jinggui Fang.

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All authors declare that they have no conflict of interest.

Research involving human and animal participants

This article does not contain any studies/data regarding human participants or animals performed by any of the authors. The study is purely based on plants’ molecular investigation.

Additional information

Communicated by S. Hohmann.

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Cui, M., Wang, C., Zhang, W. et al. Characterization of Vv-miR156: Vv-SPL pairs involved in the modulation of grape berry development and ripening. Mol Genet Genomics 293, 1333–1354 (2018). https://doi.org/10.1007/s00438-018-1462-1

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