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Transcriptome Characterization of Gene Profiling During Early Stage of Nitric Oxide-Induced Adventitious Rooting in Mung Bean Seedlings

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Abstract

Nitric oxide (NO) functions as a signaling molecule modulating diverse developmental and physiological processes in plants. NO was recently shown to strongly induce the formation of adventitious roots in plants. A transcriptome analysis was performed using RNA-Seq and qRT-PCR technologies to obtain further insights into the gene expression profile underlying NO-induced adventitious rooting. Sodium nitroprusside (SNP), a widely used NO donor, significantly up-regulated the GO terms and pathways oxidoreductase activity, wounding response, water deprivation response, microtubule-based process, cell cycle, cell wall synthesis, photosynthesis, hydrolase activity at the root induction stage, response to stress, cell wall loosening and biogenesis, ethylene signaling at the root initiation stage. In total, 2582 and 2588 differentially expressed genes (DEGs, fold change ≥ 2) were selected in plants receiving the 6- and 24-h SNP treatments, respectively. The analysis of the most highly differentially expressed genes (RPKM ≥ 10 and fold change ≥ 2) shows that NO significantly regulated the expression of genes involved in nitrogen compound response, stress response, oxidative stress response, cell wall modification, signal transduction, protein processing, secondary metabolism, metabolic processes, and transcription factors (TFs), as well as plant hormone signaling. Notably, the expression of a large number of genes encoding peroxidase (POD) isoforms was significantly differentially regulated by SNP. Furthermore, qRT-PCR results indicated that NO significantly up-regulated the expression of several genes with known functions in pathways such as auxin signaling and stress response, as well as TF genes, at the root induction and initiation stages. The evidence obtained implies that NO up-regulated the expression of genes that are involved in the key cellular processes leading to the root formation.

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Availability of Data and Materials

The unigene sequence information of this article is available in the Transcriptome Shotgun Assembly Sequence Database (http://www.ncbi.nih. gov/genbank/tsa.html) at DDBJ/EMBL/GenBank under the sequence read archive SRR 1653637 and the accession numbers GBXO01000001-GBXO01078617. The datasets supporting the conclusions of this article are included within the article and its additional files.

Abbreviations

ABA:

ABSCISIC ACID

ACC:

1-Aminocyclopropane-1-carboxylic acid

ACO:

1-Aminocyclopropane-1-carboxylic acid oxidase

ACS:

1-Aminocyclopropane-1-carboxylic acid synthase

AHK:

Arabidopsis histidine kinase

AOX:

Alternative oxidase

AP2/ERF:

Apetala2/Ethylene response factor

APX:

Ascorbate peroxidase

ARF:

Auxin response factor

AUX1/LAX:

Auxin/IAA

BR:

Brassinosteroid

BRI1:

Brassinosteroid insensitive 1

BAK1:

Brassinosteroid insensitive 1-associated receptor kinase 1-like

bHLH:

Basic/helix-loop-helix

bZIP:

Basic leucine zipper

CASPL:

Casparian strip membrane protein-like

CAT:

Catalase

cGMP:

Cyclic guanosine monophosphate

CHS:

Chalcone synthase

DEGs:

Differentially expressed genes

DHAR:

DHA reductase

Dof:

Dof zinc finger protein

EBF1:

EIN3-binding F-box protein 1-like

EIN:

Ethylene-insensitive protein

ETO:

Ethylene-overproduction protein

GA2/3OX2:

Gibberellin 2/3-beta-dioxygenase

GA2/20OX:

Gibberellins 2/20 oxidase

GATA:

GATA transcription factor

GH:

Glycoside hydrolase

GH3:

Gretchen hagen 3

GO:

Gene ontology

GPX:

Glutathione peroxidase

GR:

Glutathione reductase

GST:

Glutathione S-transferase

HD-Zip:

Homeobox-leucine zipper protein

HSPs:

Heat shock proteins

HSFs:

Heat shock transcription factors

IBA:

Indole-3-butyric acid

KAAS:

Automatic annotation server

KEGG:

Kyoto encyclopedia of genes and genomes

KOG:

Clusters of orthologous groups for eukaryotic complete genomes

LBD:

Lateral organ boundaries-domain

LEA:

Late embryogenesis abundant

LOB:

Lateral organ boundaries

LRR:

Leucine-rich repeat

MAPK:

Mitogen-activated protein kinase

MDAR:

Monodehydroascorbate reductase

NAC:

NAM, ATAF, and CUC2

NAM:

No apical meristem

NO:

Nitric oxide

NR:

NCBI non-redundant protein

PER:

Peroxidase

PIN:

PIN-formed

POD:

Peroxidase

QORL:

Quinone oxidoreductase-like protein

qRT-PCR:

Real-time quantitative polymerase chain reaction

RAM:

Root apical meristem

RNA-seq:

RNA-sequencing

ROS:

Reactive oxygen species

RPKM:

Reads per kb per million reads

SAM:

S-adenosylmethionine

SNP:

Sodium nitroprusside

SOD:

Superoxide dismutase

TFs:

Transcription factors

WRKY:

WRKYGQK domain protein

ZF:

Zinc finger protein

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Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (31760110 and 31560121).

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Authors and Affiliations

  1. School of Environmental and Municipal Engineering, Key Laboratory of Extreme Environmental Microbial Resources and Engineering, Gansu Province, Lanzhou Jiaotong University, 88 West Anning Road, Lanzhou, 730070, People’s Republic of China

    Shi-Weng Li, Yan Leng & Rui-Fang Shi

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  1. Shi-Weng Li
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  2. Yan Leng
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  3. Rui-Fang Shi
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Contributions

LSW conceived and designed the experimental plan, analyzed, and interpreted the sequence data, and drafted the manuscript. LY and SRF performed the experiments and analyzed the sequence data. All authors read and approved the final manuscript.

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Correspondence to Shi-Weng Li.

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Supplementary material 1 (PDF 107 kb)

Supplementary material 2 (XLSX 49 kb). Table S2: Top list of the differentially regulated GOs

Supplementary material 3 (XLSX 15 kb). Table S3: Top list of the differentially regulated KOs

Supplementary material 4 (XLSX 56 kb). Table S4: List of DEGs in the sample pair NO6 vs. Wat6

Supplementary material 5 (XLSX 54 kb). Table S5: List of DEGs in the sample pair NO24 vs. Wat24

Supplementary material 6 (XLSX 24 kb). Table S6: List of differentially expressed genes of transcription factors

344_2019_9993_MOESM7_ESM.xlsx

Supplementary material 7 (XLSX 12 kb). Table S7: List of differentially expressed genes associated with plant hormone signaling

Supplementary material 8 (PDF 130 kb). Table S8: Comparation of DEGs that respond to SNP and IBA

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Li, SW., Leng, Y. & Shi, RF. Transcriptome Characterization of Gene Profiling During Early Stage of Nitric Oxide-Induced Adventitious Rooting in Mung Bean Seedlings. J Plant Growth Regul 39, 430–455 (2020). https://doi.org/10.1007/s00344-019-09993-y

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  • DOI: https://doi.org/10.1007/s00344-019-09993-y

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