Preferentially expressed endosperm genes reveal unique activities in wheat endosperm during grain filling

Abstract

Background: Bread wheat (Triticum aestivum L.) endosperm contains starch and proteins, which determine the final yield, quality, and nutritional value of wheat grain. The preferentially expressed endosperm genes can precisely provide targets in the endosperm for improving wheat grain quality and nutrition using modern bioengineering technologies. However, the genes specifically expressed in developing endosperms remain largely unknown.

Results: In this study, 315 preferentially expressed endosperm genes (PEEGs) in the spring wheat landrace, Chinese Spring, were screened using data obtained from an open bioinformatics database, which reveals a unique grain reserve deposition process and special signal transduction in a developing wheat endosperm. Furthermore, transcription and accumulation of storage proteins in the wheat cultivar, XC26 were evaluated. The results revealed that 315 PEEG plays a critical role in storage protein fragment deposition and is a potential candidate for modifying grain quality and nutrition.

Conclusion: These results provide new insights into endosperm development and candidate genes and promoters for improving wheat grain quality through genetic engineering and plant breeding techniques.

Keywords: Developmental transcription; Endosperm; Storage protein; Wheat.

Fig. 1

Expression of preferentially expressed endosperm genes in Chinese Spring (CS) wheat. (A) Expression patterns of preferentially expressed endosperm genes. Each row indicates an organization. Abbreviations: DPA, days post-anthesis; WE, whole endosperm; SE, starchy endosperm. (B) Expression pattern classification of preferentially expressed endosperm genes. The x-axis represents days after flowering and the y-axis represents relative gene expression levels. Yellow or green lines indicate genes with low numbers, red and purple lines indicate genes with high numbers. (C) Detection of four genes with the highest expression level by quantitative real-time PCR. The x-axis represents different wheat plant parts and the y-axis represents the relative gene expression levels. Error bars represent standard deviations of five replicates (Chinese Spring, CS of 20 DPA)

Fig. 2

Composition and distribution of preferentially expressed endosperm genes in Chinese spring and Xinchun 26. (A) The abundance ratios of 315 gene transcripts to total transcripts from Chinese spring and Xinchun 26. (B) The composition of preferentially expressed endosperm genes. Different parts of the pie chart represent various proteins encoded by preferentially expressed endosperm genes, including other genes that are divided into four categories. (C) Expression patterns of storage protein and defense genes in the wheat genome. Each row represents a wheat plant part. Abbreviations: EPSG, endosperm-preferred storage genes; NEPSG, non-endosperm-preferred storage genes; EPDG endosperm-preferred defense genes; NEPDG, non-endosperm-preferred defense genes

Fig. 3

Transcript abundance ratios of defense-related genes in Chinese Spring and Xinchun 26. (A) Transcript abundance ratios of defense-related genes in Chinese Spring wheat. The x-axis represents the grain filling stage and the y-axis represents the ratio of each protein transcript to the total endosperm transcripts. Blue, orange, and red represent the transcript abundance of defense-related genes, redox-related genes, and proteinase inhibitors, respectively. (B) Transcript abundance ratios of defense-related genes in Xinchun 26 wheat. The x-axis represents the distinct stages of grain filling and the y-axis represents the ratio of each storage protein transcript to the total endosperm transcripts. Blue, orange, and red represent the transcript abundance of defense-related genes, redox-related genes, and proteinase inhibitors, respectively

Fig. 4

Expression levels of special signaling genes and transcription factors in Chinese Spring and Xinchun 26. (A) The expression levels of special signaling genes during the developmental stages of Chinese Spring (left) and Xinchun 26 (right) endosperms. The x-axis represents the different stages of grain filling and the y-axis represents the expression levels of signaling genes. Blue, red, and green represent the expression levels of glutamate receptors, ABA receptors, and development-related hormone receptors, respectively. (B) Expression levels of transcription factors in Chinese Spring (left) and Xinchun 26 (right) wheat. The x-axis represents the different stages of grain filling and the y-axis represents the expression levels of transcription factors. Purple, green, and orange represent the expression levels of NAC TFs, ERFs, and PLATZ TFs, respectively. Abbreviations: ABA, abscisic acid; TFs, transcription factors; ERFs, estrogen receptors

Fig. 5

Transcript abundances and expression of storage proteins. (A) Transcript abundance ratios of storage proteins in Chinese Spring and Xinchun 26, and storage protein content in Xinchun 26. (B) Transcript abundance ratios of four types of storage proteins (albumin, globulin, gliadin, and glutenin) in Chinese Spring and Xinchun 26, and the storage protein content of Xinchun 26. (C) A heatmap representing the expression levels (in transcripts per million, TPM) in samples obtained at different grain filling stages. Early, early grain filling stage; expression of storage proteins in Chinese Spring at 2 DPA (left) and in Xinchun 26 at 7 DPA (right). Medium, middle grain filling stage; the average expression of storage proteins in Chinese Spring at 10 DPA and 20 DPA (left); the average expression of storage proteins in Xinchun 26 at 7 DPA and 14 DPA (right). Late, late grain filling stage; expression of storage proteins in Chinese Spring at 30 DPA. Abbreviations: DPA, days post-anthesis