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The cell cycle arrested results in the premature advent of apical leaflets development cessation in Zygophyllum xanthoxylon

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Abstract

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An interesting but unattended phenomenon that apical leaflets growth procedure aborts early in Zygophyllum xanthoxylon was focused and shed light on from the combined different lines of evidence in the present research.

Abstract

Zygophyllum xanthoxylon, which belongs to Zygophyllaceae, is a xerophytic species exclusively distributing in Central Asia, and an appealing natural resource for researching drought-resistant strategies in the harsh environments of deserts. Morphologically, the arrest of apical leaflets growth in the early stage whether under water-starved conditions in the wilderness or in the moist conservatory is one of the drought-resistant phenotypes. However, the knowledge about stunted apical leaflets is enshrouded. Herein, we explored the potential mechanism underlying apical leaflets growth of Z. xanthoxylon combining anatomical and transcriptome sequencing technology. The anatomical results and statistics on cell number showed that the cessation of apical leaflets development is directly caused by the decreased cell number due to obstructed cell division. High-quality RNA was extracted and mixed to construct a 1–6 k library (two cells), and a total of 20.45 Gb clean data and 13,390 non-redundant full-length non-chimeric (FLNC) sequences were captured, containing 145 alternatively spliced (AS) isoforms, and 148 long non-coding RNAs (lncRNAs). The next-generation sequencing analysis of 7-d (growing stage of apical leaflets) and 40-d (blastocolysis stage of apical leaflets) apical leaflets identified 2923 differentially expressed transcripts (DETs). Furthermore, we found that the expression of GRF1, RGA1, ARR5, CRF2, TCP22 and KNOLLE genes related to cell proliferation among the DETs is significantly distinguishing between the two development periods. These genes inhibit the cell division to decrease the number of cells in the apical leaflets, but do not undergo AS events. In addition, some key lncRNAs were also found to be involved in regulating apical leaflets size. Our transcriptome data provide an effective genetic resource to further find out the code of leaf development in Z. xanthoxylon.

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Data availability

The transcriptome datasets generated and analyzed during the current study, including full-length transcriptome and Illumina sequencing reads, are available in the BioProject database of National Center for Biotechnology Information (accession number PRJNA718354).

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Acknowledgements

The authors would like to thank Dr. Liu Weizhong for sharing equipment in his laboratory. We are also grateful to the anonymous reviewers for their constructive comments on the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (grant no. 41571499, 42071067 and 32100170) and the Graduate Science and Technology Innovation Program of Shanxi Normal University (grant no. 2019XSY017).

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Correspondence to Linjing Zhang.

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468_2021_2252_MOESM1_ESM.docx

Supplementary file1 Table S1. Illumina sequencing data assessment. Table S2. The assembly results of unigenes. Table S3. Primer sequences of DETs used in qRT-PCR. Table S4. Primer sequences of lncRNAs used in qRT-PCR. Fig. S1 Summary of PacBio single-molecule real-time (SMRT) full-length transcriptome sequencing (FLT-seq) data processing a Circular consensus sequence (CCS) length distribution of cDNA library. b CCS full pass distribution. c Full-length non-chimeric (FLNC) read length distribution obtained from 1-6k libraries. d Consensus isoform read length distribution of 1-6k libraries. Fig. S2 The results of full-length transcriptome integrity assessment. Fig. S3 Relative expression of eight transcripts related to regulating cell cycle verified by quantitative real-time PCR analysis. Fig. S4 Go annotation and KEGG pathway enrichment of transcripts with alternatively splicing (AS) (DOCX 320 KB)

Supplementary file2 Predicted alternative splicing events of Z. xanthoxylon (XLS 27 KB)

Supplementary file3 The predicted target transcripts of lncRNAs (XLS 2910 KB)

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Fu, G., Li, J., Li, L. et al. The cell cycle arrested results in the premature advent of apical leaflets development cessation in Zygophyllum xanthoxylon. Trees 37, 223–237 (2023). https://doi.org/10.1007/s00468-021-02252-2

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  • DOI: https://doi.org/10.1007/s00468-021-02252-2

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