Drought stress-induced the formation of heteromorphic leaves of Populus euphratica Oliv: evidence from gene transcriptome

Abstract

Populus euphratica Oliv., a dominant species of arid desert community, grows heteromorphic leaves at different crown positions. Whether heteromorphic leaves are a strategy of plant adaptation to drought stress is rarely reported. This study sequenced the transcriptome of three typical heteromorphic leaves (lanceolate, ovate and broad-ovate leaves) of P. euphratica, and measured their drought stress. We wanted to reveal the molecular mechanisms underlying the formation of heteromorphic leaves. Drought stress was increased significantly from lanceolate to ovate to broad-ovate leaves. Gene ontology (GO) and KEGG enrichment analysis showed that the MADs-box gene regulated the expression of peroxidase (POD) in the phenylpropane biosynthetic pathway. The up-regulated expression of the chalcone synthase (CHS) gene in broad-ovate leaves significantly activated the flavonoid biosynthetic pathway. In the process of leaf shape change, the different expressions of homeodomain leucine zipper (HD-ZIP) among the three heteromorphic leaves had potential interactions on the AUX and ABA pathways. The expression of Sucrose phosphate synthase (SPS) and sucrose synthase (SUS) increased from lanceolate to broad-ovate leaves, resulting in a consistent change in starch and sucrose content. We concluded that these resistance-related pathways are expressed in parallel with leaf formation genes, thereby inducing the formation of heteromorphic leaves. Our work provided a new insights for desert plants to adapt to drought stress.

Keywords: RNA-seq; arid desert; drought stress; genetic expression; heteromorphic leaves.

Figure 1

Spatial distribution of three types of heteromorphic leaves.

Figure 2

Difference in DEGs among three heteromorphic leaves. (A) Differential gene distribution. Red, green and blue dots indicated genes are up-regulated, down-regulated and no significant differential expression, respectively. (B) Number of DEGs in the pairwise group. The a-c indicate the lanceolate-ovate, lanceolate-broad-ovate, and ovate-broad-ovate DEGs pairwise group, respectively. (C) Overall FPKM hierarchical clustering heat map. Red and blue indicate the genes with high and low expression, respectively. The color change from red to blue indicates a change in the log₁₀(FPKM+1) from large to small. LL, OL and LBL are lanceolate, ovate and broad-ovate leaves.

Figure 3

Expression difference in genes associated with plant growth and development among three heteromorphic leaves. A, B and C is the lanceolate, ovate and broad-ovate leaves, respectively. The Y-axis represents the difference between the expression (FPKM) of the corresponding genes among three heteromorphic leaves. (A–F) are genes related to cell wall organization or biogenesis, cell wall modification, pectinesterase activity, encoding ACP activity, cell division and photosynthesis, respectively.

Figure 4

Statistics of KEGG pathway enrichment. High and low values are showed in red and green, respectively. (A–C) indicate the lanceolate-ovate, lanceolate-broad-ovate, and ovate-broad-ovate DEGs pairwise group, respectively.

Figure 5

DEGs associated with the phenylpropane biosynthetic pathway in three heteromorphic leaves. The colored squares next to each gene are heat maps of the expression of key enzyme genes for the phenylpropane biosynthesis. LL, OL and LBL are lanceolate, ovate and broad-ovate leaves.

Figure 6

DEGs associated with the flavonoid biosynthesis pathway in three heteromorphic leaves. The colored squares next to each gene are heat maps of the expression of key enzyme genes for the flavonoid biosynthesis. LL, OL and LBL are lanceolate, ovate and broad-ovate leaves.

Figure 7

DEGs associated with the plant hormone signaling pathway in three heteromorphic leaves. The colored squares next to each gene are heat maps of the expression of key enzyme genes for the plant hormone signaling. LL, OL and LBL are lanceolate, ovate and broad-ovate leaves.

Figure 8

DEGs associated with the starch and sucrose metabolism pathway in three heteromorphic leaves. The colored squares next to each gene are heat maps of the expression of key enzyme genes for the starch and sucrose metabolism. LL, OL and LBL are lanceolate, ovate and broad-ovate leaves.