Transcriptome Analysis Reveals Potential Mechanism in Storage Protein Trafficking within Developing Grains of Common Wheat

Zeeshan Ali Buttar; Abdullah Shalmani; Mohsin Niaz; Chaojie Wang; Shahid Hussain; Chengshe Wang

doi:10.3390/ijms232314851

Transcriptome Analysis Reveals Potential Mechanism in Storage Protein Trafficking within Developing Grains of Common Wheat

Int J Mol Sci. 2022 Nov 27;23(23):14851. doi: 10.3390/ijms232314851.

Authors

Zeeshan Ali Buttar^{1

2}, Abdullah Shalmani³, Mohsin Niaz⁴, Chaojie Wang¹, Shahid Hussain⁵, Chengshe Wang¹

Affiliations

¹ State Key Laboratory of Crop Stress Biology in Arid Areas, College of Agronomy, Northwest A & F University, Xianyang 712100, China.
² State Key Laboratory of Wheat and Maize Crop Science, College of Agronomy, Center for Crop Genome Engineering, Longzi Lake Campus, Henan Agricultural University, Zhengzhou 450046, China.
³ College of Life Sciences, Northwest A & F University, Xianyang 712100, China.
⁴ CIMMYT-China Joint Center of Wheat and Maize Improvement, National Key Laboratory of Wheat and Maize Crop Science, Agronomy College, Henan Agricultural University, Zhengzhou 450046, China.
⁵ Jiangsu Key Laboratory of Crop Genetics and Physiology, Jiangsu Key Laboratory of Crop Cultivation and Physiology, Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Research Institute of Rice Industrial Engineering Technology, Yangzhou University, Yangzhou 225009, China.

Abstract

Gluten proteins are the major storage protein fraction in the mature wheat grain. They are restricted to the starchy endosperm, which defines the viscoelastic properties of wheat dough. The synthesis of these storage proteins is controlled by the endoplasmic reticulum (ER) and is directed into the vacuole via the Golgi apparatus. In the present study, transcriptome analysis was used to explore the potential mechanism within critical stages of grain development of wheat cultivar "Shaannong 33" and its sister line used as the control (CK). Samples were collected at 10 DPA (days after anthesis), 14 DPA, 20 DPA, and 30 DPA for transcriptomic analysis. The comparative transcriptome analysis identified that a total of 18,875 genes were differentially expressed genes (DEGs) between grains of four groups "T10 vs. CK10, T14 vs. CK14, T20 vs. CK20, and T30 vs. CK30", including 2824 up-regulated and 5423 down-regulated genes in T30 vs. CK30. Further, the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment highlighted the maximum number of genes regulating protein processing in the endoplasmic reticulum (ER) during grain enlargement stages (10-20 DPA). In addition, KEGG database analysis reported 1362 and 788 DEGs involved in translation, ribosomal structure, biogenesis, flavonoid biosynthesis pathway and intracellular trafficking, secretion, and vesicular transport through protein processing within ER pathway (ko04141). Notably, consistent with the higher expression of intercellular storage protein trafficking genes at the initial 10 DPA, there was relatively low expression at later stages. Expression levels of nine randomly selected genes were verified by qRT-PCR, which were consistent with the transcriptome data. These data suggested that the initial stages of "cell division" played a significant role in protein quality control within the ER, thus maintaining the protein quality characteristics at grain maturity. Furthermore, our data suggested that the protein synthesis, folding, and trafficking pathways directed by a different number of genes during the grain enlargement stage contributed to the observed high-quality characteristics of gluten protein in Shaannong 33 (Triticum aestivum L.).

Keywords: gene expression; grain storage protein (gluten); wheat (Triticum aestivum L.).

MeSH terms

Edible Grain / metabolism
Gene Expression Profiling*
Gene Expression Regulation, Plant
Glutens / genetics
Glutens / metabolism
Plant Proteins / genetics
Plant Proteins / metabolism
Protein Transport
Transcriptome
Triticum* / metabolism

Substances

Glutens
Plant Proteins

Grants and funding

This work was financially supported by the National Key Research and Development Program of China (2016YFD0102101), the Chinese Universities Scientific Fund (2452022112), the National Natural Science Foundation of China (31101139), and the special fund of Nanyang wheat experimental and Demonstration Station (2022NY).