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The mobile RNAs, StBEL11 and StBEL29, suppress growth of tubers in potato

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Abstract

Key message

We demonstrate that RNAs of StBEL11 and StBEL29 are phloem-mobile and function antagonistically to the growth-promoting characteristics of StBEL5 in potato. Both these RNAs appear to inhibit tuber growth by repressing the activity of target genes of StBEL5 in potato. Moreover, upstream sequence driving GUS expression in transgenic potato lines demonstrated that both StBEL11 and -29 promoter activity is robust in leaf veins, petioles, stems, and vascular tissues and induced by short days in leaves and stolons. Steady-state levels of their mRNAs were also enhanced by short-day conditions in selective organs.

Abstract

There are thirteen functional BEL1-like genes in potato that encode for a family of transcription factors (TF) ubiquitous in the plant kingdom. These BEL1 TFs work in tandem with KNOTTED1-types to regulate the expression of numerous target genes involved in hormone metabolism and growth processes. One of the StBELs, StBEL5, functions as a long-distance mRNA signal that is transcribed in leaves and moves into roots and stolons to stimulate growth. The two most closely related StBELs to StBEL5 are StBEL11 and -29. Together these three genes make up more than 70% of all StBEL transcripts present throughout the potato plant. They share a number of common features, suggesting they may be co-functional in tuber development. Upstream sequence driving GUS expression in transgenic potato lines demonstrated that both StBEL11 and -29 promoter activity is robust in leaf veins, petioles, stems, and vascular tissues and induced by short-days in leaves and stolons. Steady-state levels of their mRNAs were also enhanced by short-day conditions in specific organs. Using a transgenic approach and heterografting experiments, we show that both these StBELs inhibit growth in correlation with the long distance transport of their mRNAs from leaves to roots and stolons, whereas suppression lines of these two RNAs exhibited enhanced tuber yields. In summary, our results indicate that the RNAs of StBEL11 and StBEL29 are phloem-mobile and function antagonistically to the growth-promoting characteristics of StBEL5. Both these RNAs appear to inhibit growth in tubers by repressing the activity of target genes of StBEL5.

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Abbreviations

BELL:

BEL1-like transcription factor

BRAVO:

Brassinosteroids at vascular and organizing center

CLV:

Clavata

FT:

Flowering locus T

GA:

Gibberellin

GAS:

Galactinol synthase

GSP:

Gene-specific primers

GUS:

β-Glucoronidase

KNOX:

KNOTTED1-like Homeobox transcription factor

LD:

Long-day

OE:

Overexpression

POTH1:

Potato homeobox 1

PTB:

Polypyrimidine tract-binding protein

QC:

Quiescent centre

SAM:

Shoot apical meristem

SD:

Short-day

TALE:

Three amino acid loop extension family of proteins

TF:

Transcription factor

TFL1:

Terminal flower 1

UTR:

Untranslated region

WOX5:

WUSCHEL-RELATED HOMEOBOX5

WUS:

WUSCHEL

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Acknowledgements

Banerjee lab members gratefully acknowledge the support and core funding from Indian Institute of Science Education and Research (IISER Pune), and Department of Science and Technology (DST), Govt. of India (Grant No. SR/SO/PS-28/2010). KK acknowledge the fellowship provided by the Department of Biotechnology (DBT), India. We also thank Dr. M. M. Jana and Mr. Nitish Lahigude of IISER Pune for their help in plant maintenance in growth chambers. Contributions of the Hannapel lab were supported by the National Science Foundation Plant Genome Research Program award no. DBI-0820659.

Authors’ contributions

TG, PS and KK have generated all the constructs, transgenic lines and have conducted the experiments. DH and AKB have conceived the idea and written the manuscript and all other authors have approved it.

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    1. Biology Division, Indian Institute of Science Education and Research (IISER), Dr. Homi Bhabha Road, Pune, 411008, Maharashtra, India

      Tejashree H. Ghate, Kirtikumar R. Kondhare & Anjan K. Banerjee

    2. Plant Biology Major, Iowa State University, 253 Horticulture Hall, Ames, IA, 50011-1100, USA

      Pooja Sharma & David J. Hannapel

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    1. Tejashree H. Ghate
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    Tejashree H. Ghate and Pooja Sharma have contributed equally as first authors on this manuscript.

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    Ghate, T.H., Sharma, P., Kondhare, K.R. et al. The mobile RNAs, StBEL11 and StBEL29, suppress growth of tubers in potato. Plant Mol Biol 93, 563–578 (2017). https://doi.org/10.1007/s11103-016-0582-4

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