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A ripening-induced SlGH3-2 gene regulates fruit ripening via adjusting auxin-ethylene levels in tomato (Solanum lycopersicum L.)

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Silencing of SlGH3-2 in tomato alters auxin and ethylene levels during fruit ripening and cause reduced lycopene accumulation in the transgenic fruits.

Abstract

While auxin’s role during fleshy fruit ripening is widely acknowledged to be important, the physiological functions of several ripening-induced genes, especially those involved in the maintenance of cellular auxin homeostasis, largely remain under-explored. In the present study, the updated inventory shows that 24 members constitute the Gretchen-Hagen 3 (GH3) gene family in tomato. Their characterization using an expression profiling approach revealed that SlGH3-2, a member of the group II IAA-amido synthetase, is strongly induced at the commencement of fruit ripening. Phylogenetic analysis and homology modeling revealed that SlGH3-2 is the closest homolog of pepper CcGH3 and grapevine VvGH3-1. Expression profiling revealed that the mRNA level of SlGH3-2 is inhibited in ripening mutants such as ripening-inhibitor (rin) and Never-ripe (Nr). Whereas both auxin and ethylene were found to act as positive regulators of its transcript accumulation. The fruits of 35S::SlGH3-2 RNAi lines exhibited prolonged shelf-life. Both ethylene production and lycopene accumulation were affected in the fruits of SlGH3-2 silenced lines. These observations were corroborated by the altered expression of key ethylene and carotenoid biosynthesis genes such as ACS2 and PSY1, respectively, in the RNAi lines. Additionally, the SlGH3-2 silenced line fruits had higher IAA and IBA levels at the ripening stages, and showed increased transcript accumulation of several known auxin-induced SlIAA and SlGH3 genes. Altogether, the present study suggests that SlGH3-2 influences fruit ripening in tomato via modulating ethylene and auxin crosstalk, especially during the early phase.

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Abbreviations

ARF:

Auxin response factor

CNR:

Colorless non-ripening

FUL1 and FUL2:

Fruitful homologs

GH3:

Gretchen hagen 3

GLK:

Golden like gene

IAA:

Indole-3-acetic acid

Nr:

Never-ripe

rin:

Ripening-inhibitor

RNAi :

RNA interference

TAGL1:

Tomato agamous like 1

ACS2:

1-Aminocyclopropane-1-carboxylate synthase2

ACO1:

1-Aminocyclopropane-1-carboxylate oxidase1

CRTISO:

Carotenoid isomerase

PSY1:

Phytoene synthase1

CYCB:

lycopene β-cyclase

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Acknowledgements

This work is financially supported by grants received from the Department of Science and Technology (DST), Government of India under DST INSPIRE-Faculty Award (Grant No. IFA12-LSPA-15) and UPE II-UGC and UGC-SAP FIST II support programs. The authors acknowledge DBT, New Delhi (BT/PR11671/PBD/16/828/2008) for a research grant to, Prof. Rameshwar Sharma and Y Sreelakshmi. The authors are grateful to Dr. Siddharth Satpathy, Department of English, University of Hyderabad for proofreading of the manuscript.

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  1. Thula Sravankumar and Rahul Kumar have equally contributed to this work.

Authors and Affiliations

  1. Plant Translational Research Laboratory, Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, 500046, India

    Thula Sravankumar,  Akash, NandKiran Naik & Rahul Kumar

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  1. Thula Sravankumar
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  2. Akash
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  3. NandKiran Naik
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  4. Rahul Kumar
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RK conceived the experiments. TSK, AK, NN and RK performed the experiments and analyzed the data. RK wrote the manuscript.

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Correspondence to Rahul Kumar.

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Sravankumar, T., Akash, Naik, N. et al. A ripening-induced SlGH3-2 gene regulates fruit ripening via adjusting auxin-ethylene levels in tomato (Solanum lycopersicum L.). Plant Mol Biol 98, 455–469 (2018). https://doi.org/10.1007/s11103-018-0790-1

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