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

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.

Large and stable genome edits at the sorghum alpha kafirin locus result in changes in chromatin accessibility and globally increased expression of genes encoding lysine enrichment

“…This study identified proteins that make up the composition of kernel protein bodies in maize. A second study, Shrestha et al. (2022) , performed GWAS on several kernel protein boundamino acid phenotypes in a diverse maize population ( Shrestha et al., 2022 ).…”

Elucidating the patterns of pleiotropy and its biological relevance in maize

“…Data were collected from 3,873 leaf mass features [37], 116,381 RNA expression values from seven tissues [38], and 343 field traits. Field traits included flowering time [3,69], plant architecture [21,46,[70][71][72][73][74][75], disease and insect resistance [76][77][78][79][80][81][82][83], and kernel composition [84][85][86][87][88][89][90]. Many of these traits are replicated across environments, so a single representative version of that trait was kept.…”

“…These population-trait categories were: 1) NAM field, 2) GAP field, 3) GAP mass features, and 4) GAP expression traits. Some traits within GAP field traits included kernel carotenoids and metabolites [84,86,[88][89][90], which could be classified into GAP mass features type because they are also molecular phenotypes. However, only the metabolites measured within a single study were classified as GAP mass features [37].…”

Remodelled Ribosomes Synthesise a Specific Proteome in Proliferating Plant Tissue during Cold

“…Targeted translation of mRNAs based on altered ribosomal structures is referred to as ribosome specialization ( Genuth and Barna, 2018 ; Martinez-Seidel et al, 2020 ; Slavov et al, 2015 ). Functional specialization of ribosomes entails translational events that drive a response to an external ( Lambers, 2022 ; Berková et al, 2020 ; Moin et al, 2021 ; Appels et al, 2021 ) or a developmental ( Norris et al, 2021 ; Shrestha et al, 2022 ; Xiong et al, 2021 ) cue, for example, the preferred translation of specific groups of proteins that facilitate acclimation to low temperatures. These concepts suggest that the previously observed abundance changes of the translational machinery in cold-acclimating root tips of barley seedlings ( Martinez-Seidel et al, 2021c ) may indicate the production of ribosomes tuned to cold-specialized translation.…”