Multiomics approach reveals a role of translational machinery in shaping maize kernel amino acid composition

Authors: SHRESTHA, VIVEK - University Of Missouri; YOBI, ABOU - University Of Missouri; SLATEN, MARIANNE - University Of Missouri; CHAN, YEN ON - University Of Missouri; HOLDEN, SAMUEL - University Of Missouri; GYAWALI, ABISKAR - University Of Missouri; Flint-Garcia, Sherry; LIPKA, ALEXANDER - University Of Illinois; ANGELOVICI, RUTHIE - University Of Missouri

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/21/2021
Publication Date: 1/1/2022
Citation: Shrestha, V., Yobi, A., Slaten, M.L., Chan, Y., Holden, S., Gyawali, A., Flint Garcia, S.A., Lipka, A.E., Angelovici, R. 2022. Multiomics approach reveals a role of translational machinery in shaping maize kernel amino acid composition. Plant Physiology. 188(1):111-133. https://doi.org/10.1093/plphys/kiab390.
DOI: https://doi.org/10.1093/plphys/kiab390

Interpretive Summary: Corn is an important component of food and animal feed, but is limited in several essential amino acids, including lysine, methionine, and tryptophan. Historical efforts to improve the amino acid balance in corn have been hindered by the complex mechanisms that control protein storage in the kernel. We used two complementary approaches to identify genes involved in amino acid composition and the individual proteins that accumulate and change in the kernel over the course of kernel development. Comparing the outcomes of these approaches both confirmed previously known results and identified a surprising new mechanism: 1) we verified that a particular class of kernel storage proteins (the gamma zeins) plays a key part in determining amino acid composition, and 2) unexpectedly, we also found that the basic cellular machinery responsible for translating messenger RNA into proteins also plays an extremely important role in amino acid composition in maize grain. These novel findings regarding the translational machinery suggests new and exciting avenues for maize seed amino acid biofortification. This will improve the nutritional value for human food around the world, and add value to the food and meat production supply chain by reducing the need for nutritional supplements in animal feed.

Technical Abstract: Maize (Zea mays) seeds are a good source of protein, despite being deficient in several essential amino acids. However, eliminating the highly abundant but poorly balanced seed storage proteins has revealed that the regulation of seed amino acids is complex and does not rely on only a handful of proteins. In this study, we used two complementary omics-based approaches to shed light on the genes and biological processes that underlie the regulation of seed amino acid composition. We first conducted a genome-wide association study to identify candidate genes involved in the natural variation of seed protein-bound amino acids. We then used weighted gene correlation network analysis to associate protein expression with seed amino acid composition dynamics during kernel development and maturation. We found that almost half of the proteome was significantly reduced during kernel development and maturation, including several translational machinery components such as ribosomal proteins, which strongly suggests translational reprogramming. The reduction was significantly associated with a decrease in several amino acids, including lysine and methionine, pointing to their role in shaping the seed amino acid composition. When we compared the candidate gene lists generated from both approaches, we found a nonrandom overlap of 80 genes. A functional analysis of these genes showed a tight interconnected cluster dominated by translational machinery genes, especially ribosomal proteins, further supporting the role of translation dynamics in shaping seed amino acid composition. These findings strongly suggest that seed biofortification strategies that target the translation machinery dynamics should be considered and explored further.