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. 2022 Jan 12:12:746166.
doi: 10.3389/fpls.2021.746166. eCollection 2021.

Response of Multiple Tissues to Drought Revealed by a Weighted Gene Co-Expression Network Analysis in Foxtail Millet [ Setaria italica (L.) P. Beauv.]

Renliang Zhang  1 , Hui Zhi  1 , Yuhui Li  2 , Erhu Guo  2 , Guojun Feng  3 , Sha Tang  1 , Weixia Guo  1 , Linlin Zhang  1 , Guanqing Jia  1 , Xianmin Diao  1
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Response of Multiple Tissues to Drought Revealed by a Weighted Gene Co-Expression Network Analysis in Foxtail Millet [ Setaria italica (L.) P. Beauv.]

Renliang Zhang et al. Front Plant Sci. .

Abstract

Characterization of drought-tolerance mechanisms during the jointing stage in foxtail millet under water-limited conditions is essential for improving the grain yield of this C4 crop species. In this trial, two drought-tolerant and two drought-sensitive cultivars were examined using transcriptomic dissections of three tissues (root, stem, and leaf) under naturally occurring water-limited conditions. We detected a total of 32,170 expressed genes and characterized 13,552 differentially expressed genes (DEGs) correlated with drought treatment. The majority of DEGs were identified in the root tissue, followed by leaf and stem tissues, and the number of DEGs identified in the stems of drought-sensitive cultivars was about two times higher than the drought-tolerant ones. A total of 127 differentially expressed transcription factors (DETFs) with different drought-responsive patterns were identified between drought-tolerant and drought-sensitive genotypes (including MYB, b-ZIP, ERF, and WRKY). Furthermore, a total of 34 modules were constructed for all expressed genes using a weighted gene co-expression network analysis (WGCNA), and seven modules were closely related to the drought treatment. A total of 1,343 hub genes (including RAB18, LEA14, and RD22) were detected in the drought-related module, and cell cycle and DNA replication-related transcriptional pathways were identified as vital regulators of drought tolerance in foxtail millet. The results of this study provide a comprehensive overview of how Setaria italica copes with drought-inflicted environments during the jointing stage through transcriptional regulating strategies in different organs and lays a foundation for the improvement of drought-tolerant cereal cultivars through genomic editing approaches in the future.

Keywords: RNA-Seq; Setaria italica; WGCNA; drought; jointing stage; multi-tissue.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Responses of drought-tolerant and sensitive accessions toward water-limited conditions at the jointing stage. (A) A decrease in grain weight and plant height in 10 diverse accessions under water-limited conditions during the jointing stage; (B–F) leaf-relative water contents (B), leaf water potential (C), soluble sugar content (D), photosynthetic rate (E), and stomatal conductance (F) of drought-sensitive and drought-tolerant cultivars under both normal and drought-stressed conditions; (G–J) morphological phenotypes of spreading leaves after drought treatments in drought-sensitive and drought-tolerant accessions. Ci134 (G) and Ci603 (H) are drought-sensitive genotypes, while Ci328 (I) and Ci409 (J) are drought tolerant. Bar = 10 cm. * represents p < 0.05 determined by Student's t-test, ** represents p < 0.01 determined by Student's t-test.
Figure 2
Figure 2
A summary of differentially expressed genes detected in this trial. (A) Distributions of log10 (counts); (B) density of log10 (FPKM); (C) PCA analysis of each RNA-seq sample. (D) Number of DEGs responding to drought treatment in each sample. Drought-tolerant genotypes are Ci328 and Ci409; drought-sensitive genotypes are Ci134 and Ci603. NO represents the normal condition, and DR represents drought treatments.
Figure 3
Figure 3
Comparisons of DEGs from three tissues of four foxtail millet accessions. Venn diagrams of shared DEGs among different genotypes (A: Ci134; B: Ci603; C: Ci328; D: Ci409) and different tissues (E: root; F: stem; and G: leaf). Drought-tolerant genotypes: Ci328 and Ci409; drought-sensitive genotypes: Ci134 and Ci603. Numbers in parentheses represent total DEGs.
Figure 4
Figure 4
Twenty-one oppositely regulated DEGs were identified in drought-tolerant and drought-sensitive genotypes under water-limited conditions. Cell color represents the expression pattern of relevant DEGs in all three tissues of four accessions. Red represents an upregulated pattern, while blue represents a downregulated pattern. Four, one, and 16 oppositely expressed DEGs responding to drought between drought-sensitive/tolerant accessions that were identified in roots, stems, and leaves, respectively.
Figure 5
Figure 5
Enrichment of differentially expressed transcription factors (DETFs) identified in three tissues of all four accessions. Each column represents a gene set. The circle size represents the gene ratio, and the circle color represents the P-value. The number in the middle of each circle represents the numbers of DETFs annotated in each GO term or KEGG pathway.
Figure 6
Figure 6
K-means clustering of DEGs identified in three tissues of four foxtail millet accessions. K-means clusters of DEGs in roots (A), stems (B), and leaves (C) across all four accessions. NO refers to normal, and DR refers to drought conditions. Numbers in parentheses represent the numbers of DEGs found in each cluster. The y axis represents normalized gene expression. Red and brown refer to normal and drought treatment of drought-sensitive genotypes, respectively. Green and blue refer to normal and drought treatment of drought-tolerant genotypes.
Figure 7
Figure 7
Drought-induced DEGs between genotypes (di-DBG) identified between tolerant and sensitive genotypes. (A) The definition and identification of di-DBG. (B,C) GO (B) and KEGG (C) enrichment analysis of di-DBG in leaves and roots.
Figure 8
Figure 8
Eigengene expression and the regulatory network of DEGs in drought-correlated modules identified through the WGCNA approach. (A,B) Eigengene expression (A) and network (B) of the purple module; (C,D) Eigengene expression (C) and the network (D) of the purple module; (E,F) Eigengene expression (E) and the network (F) of the light yellow module; (G,H) Eigengene expression (G) and the network (H) of the turquoise module.
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References

    1. Adams S., Grundy J., Veflingstad S. R., Dyer N. P., Hannah M. A., Ott S., et al. . (2018). Circadian control of abscisic acid biosynthesis and signalling pathways revealed by genome-wide analysis of LHY binding targets. New Phytol. 220, 893–907. 10.1111/nph.15415 - DOI - PubMed
    1. Ali M. A., Plattner S., Radakovic Z., Wieczorek K., Elashry A., Grundler F. M., et al. . (2013). An Arabidopsis ATPase gene involved in nematode-induced syncytium development and abiotic stress responses. Plant J. 74, 852–866. 10.1111/tpj.12170 - DOI - PMC - PubMed
    1. Angeles-Núñez J. G., Tiessen A. (2012). Regulation of AtSUS2 and AtSUS3 by glucose and the transcription factor LEC2 in different tissues and at different stages of Arabidopsis seed development. Plant Mol. Biol. 78, 377–392. 10.1007/s11103-011-9871-0 - DOI - PubMed
    1. Arisz S. A., Heo J. Y., Koevoets I. T., Zhao T., van Egmond P., Meyer A. J., et al. . (2018). DIACYLGLYCEROLACYLTRANSFERASE1 contributes to freezing tolerance. Plant Physiol. 177, 1410–1424. 10.1104/pp.18.00503 - DOI - PMC - PubMed
    1. Ault T. R.. (2020). On the essentials of drought in a changing climate. Science 368, 256–260. 10.1126/science.aaz5492 - DOI - PubMed