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Evolution of the Tóxicos en Levadura 63 (TL63) gene family in plants and functional characterization of Arabidopsis thaliana TL63 under oxidative stress

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Abstract

Main conclusion

TL63 orthologs were angiosperm specific and had undergone motifs loss and gain, and increased purifying selection. AtTL63 was involved in the response of yeast and Arabidopsis plants to oxidative stress.

Abstract

The Tóxicos en Levadura (TL) family, a class of E3 ubiquitin ligases with typical RING-H2 type zinc finger structure, plays a pivotal role in mediating physiological processes and responding to stress in plants. However, the evolution and function of TL63 remain unclear. In this study, TL63 homologs were dated roughly back to the origin of land plants and confirmed to have subjected to the gain and loss of motifs and increased purifying selection. Phylogenetic analysis displayed that 279 TL63s could be divided into four main clades (Clade A-D). Notably, the ancestral tandem TL40/41 cluster contributed to the expansion of modern Brassicaceae TL40/41. The substitution rate tests revealed that the TL63 lineage was evidently different from other lineages. The codon usage index exhibited that monocotyledons preferred to use not A3s and T3s, but C3s, G3s, CAI, CBI and Fop. Sequence analysis showed that the TL63 homologs had conserved TM and GLD motifs and RING-H2 domain whose key amino acid residues accounted for the high average abundance. Particularly, Arabidopsis thaliana TL63 (AtTL63) was located in the nuclei, cell membranes and peroxisomes and expressed universally and significantly throughout A. thaliana development. Under H2O2 treatment, low or moderate expression of the AtTL63 held beneficial effects on the growth and viability of yeast cells and the mutation or overexpression of the AtTL63 positively affected the growth of A. thaliana plants. In brief, this study could supply useful insight into the evolution of the plant TL63s and the AtTL63 functions under oxidative stress.

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Data availability

All the data generated in this study are included in this publishing article and its supplementary information. Further inquiries can be directed to the corresponding author.

Abbreviations

TL:

Tóxicos en Levadura

ROS:

Reactive oxygen species

WGDs:

Whole genome duplications

ώ = dN/dS :

 Nonsynonymous/synonymous substitutions

RSCU:

Relative synonymous codon usage

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Funding

This research was supported by the Shanghai Sailing Program (19YF1414800) to Min Jiang. The funding body had no role in study design, analysis, decision to publish, or preparation of the manuscript.

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  1. Peng Li and Yuxin Zhang contributed equally to this work.

Authors and Affiliations

  1. Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, 200438, China

    Peng Li, Yuxin Zhang & Min Jiang

  2. Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai, 201602, China

    Peng Li & Min Jiang

  3. College of Agronomy and Biotechnology, Yunnan Agricultural University, Kunming, 650201, China

    Changling Zhao

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  1. Peng Li
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Contributions

MJ and CZ conceived and designed the experiments. PL and YZ performed most of the experiments and analyzed the data. MJ, PL and YZ wrote the manuscript. MJ and CZ reviewed and edited the manuscript. All authors read and approved the final manuscript.

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Correspondence to Changling Zhao or Min Jiang.

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425_2023_4243_MOESM1_ESM.pdf

Fig. S1 Sequence logos of the conserved (a) and unique (b) domains/motifs in TL63 homologs. The height of the letter indicates its relative frequency at the given position (x -axis) in the domain/motif. (PDF 2516 KB)

425_2023_4243_MOESM2_ESM.pdf

Fig. S2 Sequence features of TM (a), GLD (b) and RING (c) motifs of TL63s in different phylogenetic groups. The red star indicates residues of functional or structural importance based on phylogenetic conservations. (PDF 1266 KB)

425_2023_4243_MOESM3_ESM.pdf

Fig. S3 Determination of the relative AtTL63 expression level. a The expression of AtTL63 in control (pREP41 and pREP81), pREP41- AtTL63 and pREP81- AtTL63 yeast cells, grown in normal condition, assessed by real-time PCR. Values are means ±SD of three independent experiments. Student’s t test was performed (**P < 0.01). b The expression of AtTL63 in wild type (WT), tl63 and AtTL63-OE plants. Experiments were conducted for three biological replicates. Data are the means of ±SD. Student’s t test was performed (**P < 0.01). (PDF 3524 KB)

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Li, P., Zhang, Y., Zhao, C. et al. Evolution of the Tóxicos en Levadura 63 (TL63) gene family in plants and functional characterization of Arabidopsis thaliana TL63 under oxidative stress. Planta 258, 87 (2023). https://doi.org/10.1007/s00425-023-04243-8

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