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Transcriptomic analyses reveal the effect of nitric oxide on the lateral root development and growth of mangrove plant Kandelia obovata

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Abstract

Background and aims

Kandelia obovata, a dominant mangrove species in China, produces complex buttress roots and prop roots in intertidal wetlands where high quantities of nitric oxide (NO) are produced by reducing sediments. NO, a key signaling molecule, participates in an array of plant physiological and developmental processes. However, it is unclear whether NO functions in K. obovata root system establishment.

Methods

Here, we used a transcriptomic approach to investigate the potential role of NO in the regulation of K. obovata lateral root development and growth. Transcript profiles and bioinformatics analyses were used to characterize potential regulatory mechanisms.

Results

Application of exogenous sodium nitroprusside (SNP, an NO donor) enhanced K. obovata lateral root development and growth in a dose-dependent manner. Furthermore, the effects of SNP were abolished by the addition of cPTIO (NO scavenger). RNA-seq analysis identified 1,593 differentially expressed genes (DEGs), of which 646 and 947 were up- and down-regulated in roots treated with NO donor. Functional annotation analysis demonstrated that the starch and sucrose pathway was significantly induced in response to NO. A suite of DEGs involved in hormone signal transduction and cell wall metabolism was also differentially regulated by NO. Taken together, our results suggest that a complex interaction between energy metabolism, multiple hormone signaling pathways, and cell wall biosynthesis is required for the NO regulation on lateral root development and growth in mangrove plant K. obovata.

Conclusion

NO appears to contribute to the formation of the unique root system of mangrove plants.

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Acknowledgments

This work was financially supported by the National Key Research and Development Program of China (2017YFC0506102) and the Natural Science Foundation of China (NSFC) (32171740, 31870581, 31570586 and 31601133).

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Author notes

  1. Ming-Yue Wei and Huan Li contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, College of the Environment and Ecology, Xiamen University, Xiamen, Fujian, 361005, People’s Republic of China

    Ming-Yue Wei, Huan Li, You-Hui Zhong, Zhi-Jun Shen, Dong-Na Ma, Chang-Hao Gao, Yi-Ling Liu, Jing-Ya Zhang, Yan-Ping You & Hai-Lei Zheng

  2. College of Food and Bio-engineering, Bengbu University, Bengbu, Anhui, 233030, People’s Republic of China

    Huan Li

  3. Fujian Key Laboratory of Subtropical Plant Physiology and Biochemistry, Fujian Institute of Subtropical Botany, Xiamen, Fujian, 361006, People’s Republic of China

    Wen-Hua Wang

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  1. Ming-Yue Wei
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M. W., H. L. and H. Z. designed the experiments. M. W. and H. L. performed and analyzed the transcriptomic data. M. W. wrote the paper. Y. Z., C. G., D. M, Z. S, W. W, J. Z and Y. Y gave the suggestions. H. Z. revised this paper. All authors have read and approved the manuscript.

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Correspondence to Hai-Lei Zheng.

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Supplementary Information

Supplementary Fig. S1

Characteristics of homology search of unigenes against the NCBI non-redundant protein sequence (Nr) database. Similarity distribution of top BLAST hits for each unigene (A), E-value distribution of BLAST hits for each unique sequence with a cut-off E-value of 1e-5 (B), and species classification of the top BLAST hits for each unigene with a cut-off E-value of 1e-5 (C). (PNG 267 kb)

High Resolution Image (TIFF 545 kb)

Supplementary Fig. S2

COG function classification of the annotated unigenes. Unigenes are classified into 25 categories. COG functional classes are shown on the x-axis, and the percentage of a specific class of unigenes is shown on the left y-axis. (PNG 390 kb)

High Resolution Image (TIFF 1091 kb)

Supplementary Fig. S3

GO classification of the annotated unigenes. The x-axis represents the number of genes in a sub-category. The left y-axis indicates the sub-categories of annotated unigenes in three categories: biological process (red), cellular component (blue), and molecular function (green). (PNG 462 kb)

High Resolution Image (TIFF 1123 kb)

Supplementary Fig. S4

KEGG classification of the annotated unigenes. The x-axis represents the percentage of a specific sub-category of unigenes in the main category. The left y-axis represents the sub-categories of annotated unigenes in five categories: (A) cellular processes, (B) environmental information processing, (C) genetic information processing, (D) metabolism, and (E) organismal systems. (PNG 244 kb)

High Resolution Image (TIFF 641 kb)

Supplementary Table S1

Primers used in qRT-PCR analysis (DOCX 14 kb)

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Wei, MY., Li, H., Zhong, YH. et al. Transcriptomic analyses reveal the effect of nitric oxide on the lateral root development and growth of mangrove plant Kandelia obovata. Plant Soil 472, 543–564 (2022). https://doi.org/10.1007/s11104-021-05271-7

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