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Maleic hydrazide elicits global transcriptomic changes in chemically topped tobacco to influence shoot bud development

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Abstract

Main conclusion

Transcriptomic analysis revealed maleic hydrazide suppresses apical and axillary bud development by altering the expression of genes related to meristem development, cell division, DNA replication, DNA damage and recombination, and phytohormone signaling.

Abstract

Topping (removal of apical buds) is a common agricultural practice for some crop plants including cotton, cannabis, and tobacco. Maleic hydrazide (MH) is a systemic suckercide, a chemical that inhibits shoot bud growth, used to control the growth of apical (ApB) and axillary buds (AxB) following topping. However, the influence of MH on gene expression and the underlying molecular mechanism of controlling meristem development are not well studied. Our RNA sequencing analysis showed that MH significantly influences the transcriptomic landscape in ApB and AxB of chemically topped tobacco. Gene ontology (GO) enrichment analysis revealed that upregulated genes in ApB were enriched for phosphorelay signal transduction, and the regulation of transition timing from vegetative to reproductive phase, whereas downregulated genes were largely associated with meristem maintenance, cytokinin metabolism, cell wall synthesis, photosynthesis, and DNA metabolism. In MH-treated AxB, GO terms related to defense response and oxylipin metabolism were overrepresented in upregulated genes. GO terms associated with cell cycle, DNA metabolism, and cytokinin metabolism were enriched in downregulated genes. Expression of KNOX and MADS transcription factor (TF) family genes, known to be involved in meristem development, were affected in ApB and AxB by MH treatment. The promoters of MH-responsive genes are enriched for several known cis-acting elements, suggesting the involvement of a subset of TF families. Our findings suggest that MH affects shoot bud development in chemically topped tobacco by altering the expression of genes related to meristem development, DNA repair and recombination, cell division, and phytohormone signaling.

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Abbreviations

ABA:

Abscisic acid

ACO:

1-Aminocyclopropane-1-carboxylate oxidase

ACS:

1-Aminocyclopropane-1-carboxylate synthase

AGL:

Agamous-like

AOS:

Allene oxide synthase

ApB:

Apical bud

AxB:

Axillary bud

ARR:

Arabidopsis Response regulators

APRR:

Arabidopsis Pseudo-response regulators

BARD1:

Breast cancer-associated ring domain 1

BTB/POZ:

Bric-à-brac, tramtrack and broad complex/poxvirus and zinc finger

CDC:

Cell division control

Cdt1:

Chromatin licensing and DNA replication factor 1

CK:

Cytokinin

CPS:

ent-Copalyl diphosphate synthase

CRF:

Cytokinin response factor

DEG:

Differentially expressed genes

Cul4:

Uniculme4

DHAR:

Glutathione-dependent dehydroascorbate reductase

ERF:

Ethylene response factor

ET:

Ethylene

FDR:

False discovery rate

FPKM:

Fragments per kilobase of gene per million reads mapped

GA:

Gibberellin

GGDP:

Geranylgeranyl diphosphate

GAox:

GA oxidases

GO:

Gene ontology

GST:

Glutathione S-transferases

HK:

Histidine kinase

HP:

His-containing phosphotransfer protein

JA:

Jasmonic acid

KNATM:

KNOX Arabidopsis thaliana MEINOX

KNOX:

Knotted1-like homeobox

KO:

Ent-kaurine oxidase

KS:

Ent-kaurene synthase

LAS:

Lateral suppressor

MCM:

Minichromosome maintenance

MH:

Maleic hydrazide

NTPase:

Nucleotide triphosphatases

ORC:

Origin recognition complex

PR genes:

Pathogenesis-related genes

PWMs:

Position-specific weight matrices

RAX:

Regulator of axillary meristems

RIN:

RNA integrity number

REV:

Revolute

ROX:

Regulator of axillary meristem formation

RPN12A:

Regulatory particle non-atpase 12A

SA:

Salicylic acid

SAM:

Shoot apical meristem

SAMT:

Salicylic acid carboxyl methyltransferase

TB1:

Teosinte branched 1

TF:

Transcription factor

TS:

Terpene synthase

TSS:

Translation start site

TSNA:

Tobacco-specific nitrosamines

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Acknowledgements

This work is supported partially by grants from the Kentucky Tobacco Research and Development Center, University of Kentucky and The Council for Burley Tobacco, Kentucky, to L.Y. and S.P., and a Graduate Research Fellowship to M.D.R. from Department of Plant Soil Sciences, University of Kentucky.

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Authors and Affiliations

  1. Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, 40546, USA

    Mitchell D. Richmond, Robert C. Pearce, William A. Bailey & Ling Yuan

  2. Kentucky Tobacco Research and Development Center, University of Kentucky, Lexington, KY, 40546, USA

    Sanjay K. Singh, Xin Hou, Sitakanta Pattanaik & Ling Yuan

  3. Department of Tobacco, College of Plant Protection, Shandong Key Laboratory of Agricultural Microbiology, Shandong Agricultural University, Tai`an, 271018, China

    Xin Hou

  4. Canadian Tobacco Research Foundation, Tillsonburg, ON, N4G 4H5, Canada

    Mitchell D. Richmond

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  1. Sanjay K. Singh
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Correspondence to Sitakanta Pattanaik or Ling Yuan.

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Singh, S.K., Richmond, M.D., Pearce, R.C. et al. Maleic hydrazide elicits global transcriptomic changes in chemically topped tobacco to influence shoot bud development. Planta 252, 64 (2020). https://doi.org/10.1007/s00425-020-03460-9

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