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. 2022 Feb 4;11(3):429.
doi: 10.3390/plants11030429.

A Survey of Enhanced Cold Tolerance and Low-Temperature-Induced Anthocyanin Accumulation in a Novel Zoysia japonica Biotype

Hai-Xiang Jin  1   2 , Ming Jiang  1   3 , Jian-Feng Yang  2 , Zhi-Hao Wu  1   3 , Long-Long Ma  1   3 , Cong-Cong Wang  1   3 , Chen Liang  1   2   3 , Xin-Yi Ning  1   3   4 , Liang-Fa Ge  3 , Shu Chen  1
Affiliations

A Survey of Enhanced Cold Tolerance and Low-Temperature-Induced Anthocyanin Accumulation in a Novel Zoysia japonica Biotype

Hai-Xiang Jin et al. Plants (Basel). .

Abstract

Zoysia japonica is a warm-season turfgrass that is extensively used in landscaping, sports fields, and golf courses worldwide. Uncovering the low-temperature response mechanism of Z. japonica can help to accelerate the development of new cold-tolerant cultivars, which could be used to prolong the ornamental and usage duration of turf. A novel Z. japonica biotype, YueNong-9 (YN-9), was collected from northeastern China for this study. Phenotypic measurements, cold-tolerance investigation, and whole-transcriptome surveys were performed on YN-9 and LanYin-3 (LY-3), the most popular Z. japonica cultivar in Southern China. The results indicated the following: YN-9 has longer second and third leaves than LY-3; when exposed to the natural low temperature during winter in Guangzhou, YN-9 accumulated 4.74 times more anthocyanin than LY-3; after cold acclimation and freezing treatment, 83.25 ± 9.55% of YN-9 survived while all LY-3 leaves died, and the dark green color index (DGCI) value of YN-9 was 1.78 times that of LY-3; in YN-9, there was a unique up-regulation of Phenylalanine ammonia-lyase (PAL), Homeobox-leucine Zipper IV (HD-ZIP), and ATP-Binding Cassette transporter B8 (ABCB8) expressions, as well as a unique down-regulation of zinc-regulated transporters and iron-regulated transporter-like proteins (ZIPs) expression, which may promote anthocyanin biosynthesis, transport, and accumulation. In conclusion, YN-9 exhibited enhanced cold tolerance and is thus an excellent candidate for breeding cold-tolerant Z. japonica variety, and its unique low-temperature-induced anthocyanin accumulation and gene responses provide ideas and candidate genes for the study of low-temperature tolerance mechanisms and genetic engineering breeding.

Keywords: RNA-seq; abiotic stress; anthocyanin biosynthesis; anthocyanin transport; turfgrass.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Phenotypic characteristics of YN-9 Zoysia japonica: (A) shoot and rhizome; (B) inflorescence and seedhead; (C) spikelete with pedicel.
Figure 2
Figure 2
Leaf color and anthocyanin content variations in LY-3 and YN-9 after winter in Guangzhou. (a) Photos of LY-3 and YN-9 after winter in Guangzhou; (b) Anthocyanin content of LY-3 and YN-9 leaves before and after winter in Guangzhou; ** above the error bar indicates a significant difference (p-value < 0.01) between LY-3 and YN-9.
Figure 3
Figure 3
Phenotypic variations and survival rates of LY-3 and YN-009 after low-temperature treatment. (a) Photos of LY-3 and YN-9 before and after low-temperature treatment; (b) Survival rates and DGCI variations of LY-3 and YN-9 after low-temperature treatment; DGCI represents for dark green color index, ** indicates a significant difference (p-value < 0.01) between LY-3 and YN-9, CK indicates DGCI values before treatment, LT indicates DGCI values after treatment.
Figure 4
Figure 4
Venn diagram of up-regulated (log2FC >1 and p-value adjusted < 0.05) and down-regulated genes (log2FC < −1 and p-value adjusted < 0.05) of LY-3 and YN-9 after cold acclimation (CA) and freezing (FZ) treatment.
Figure 5
Figure 5
Distribution of up-regulated (log2FC > 1 and p-value adjusted < 0.05) and down-regulated genes (log2FC < −1 and p-value adjusted < 0.05) of LY-3 and YN-9 after cold acclimation (CA) and freezing (FZ) treatment in different log2FC intervals.
Figure 6
Figure 6
Expression variations and sequence structure of genes involved in pigment accumulation and auxin transmembrane transport in LY-3 and YN-9 after cold acclimation and freezing treatment. The heatmaps were drawn based on log2FC values. The grey rectangle highlighted the genes shared by GOs of pigment accumulation and auxin transmembrane transport. The protein domains were predicted with Pfam database using Interproscan.
Figure 7
Figure 7
Phylogenetic analysis of the four Zoysia japonica HD-ZIP IV proteins (in green) associated with pigmentation and 16 Arabidopsis thaliana HD-ZIP IV members (in yellow). Multiple sequence alignment was performed using MUSCLE with default settings; Phylogenetic tree was constructed using Neighbor-Joining method with 1000 bootstrap replicates.
Figure 8
Figure 8
Expression variations of anthocyanin-biosynthesis genes in LY-3 and YN-9 after cold acclimation (CA) and freezing (FZ) treatment. (A) Heatmap based on log2FC of anthocyanin-biosynthesis genes, * indicates up-regulated genes with log2FC > 1 and p-value adjusted < 0.05. (B) Global picture of anthocyanin biosynthesis in plant cells.
Figure 9
Figure 9
Expression variations and sequence structures of ZIP genes in LY-3 and YN-9 after cold acclimation and freezing treatment. The heatmaps were drawn based on log2FC values, * and ** indicate significant differences at p-values < 0.05 and 0.01, respectively. The sequence structures were drawn based on Interproscan analysis with PANTHER database.
Figure 10
Figure 10
A proposed schematic representation of how low temperature-induced fluctuations of transcript abundance regulate anthocyanin synthesis, transport, and accumulation in YN-9 leaf cells. → and ┤ indicate positive and negative regulation of biological processes, respectively.
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