Temporal regulation of metabolome and proteome in photosynthetic and photorespiratory pathways contributes to maize heterosis

Authors: LI, ZHI - University Of Texas At Austin; ZHU, ANDAN - University Of Texas At Austin; SONG, QINGXIN - University Of Texas At Austin; CHEN, HELEN - University Of Texas At Austin; Harmon, Frank; CHEN, Z. JEFFERY - University Of Texas At Austin

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/11/2020
Publication Date: 9/30/2020
Citation: Li, Z., Zhu, A., Song, Q., Chen, H.Y., Harmon, F.G., Chen, Z. 2020. Temporal regulation of metabolome and proteome in photosynthetic and photorespiratory pathways contributes to maize heterosis. The Plant Cell. 32(12):3706-3722. https://doi.org/10.1105/tpc.20.00320.
DOI: https://doi.org/10.1105/tpc.20.00320

Interpretive Summary: Heterosis or hybrid vigor is widespread in plants and animals. The beneficial effects of heterosis have been used to improve yields in a wide range of crops, including corn (also known as maize). Heterosis occurs in the first generation after interbreeding two genetically different parents. The plants of this first generation are referred to as hybrids. These hybrid plants have higher performance than their parents, which is the manifestation of heterosis. To better understand the underlying causes of heterosis, this study measured differences in the proteins (the proteome) and the metabolic products (the metabolome) of maize hybrids in comparison to the parents of these hybrids. This study found that, compared to parental maize plants, hybrid plants have higher levels of enzymes that produce beneficial metabolic products and enzymes that remove toxic metabolic byproducts. This finding correlated with more beneficial metabolites and fewer toxic ones in hybrid plants. Also, a large fraction of maize metabolites and proteins in both hybrid and parental plants appeared only at specific times during a 24-hour period, but this timing was changed in hybrid plants. This finding shows hybrid plant metabolism responds differently to environmental signals and this could be an important component of enhanced performance of hybrid plants. This study concludes that hybrids optimize metabolic product abundance to match the environment by changing when and how much of key enzymes are made, which leads to enhanced photosynthesis and plant growth. This study contributes to understanding the causes of heterosis, which can be leveraged to improve yield in maize and other crop plants.

Technical Abstract: Heterosis or hybrid vigor is widespread in plants and animals. Despite the molecular basis for heterosis has been extensively studied, metabolic and proteomic contributions to heterosis remain elusive. Here we report integrative analysis of time-series metabolome and proteome data in maize hybrids and their inbred parents. A large fraction of maize metabolites and proteins is diurnally regulated, many of which show nonadditive abundance in the hybrids, including key enzymes and metabolites involved in carbon assimilation. Compared with high levels of trait heterosis, metabolic heterosis is relatively mild. Interestingly, most amino acids display negative mid-parent heterosis (MPH), while metabolites in sugars, alcohols and nucleosides show positive MPH. From the network perspectives, metabolites in the photosynthetic pathway show positive MPH, whereas metabolites in the photorespiratory pathway show negative MPH, which correspond to nonadditive protein abundance of key enzymes in the respective pathways in the hybrids. Moreover, rhythmic proteins that are upregulated in the hybrids are enriched in photosynthetic related Gene Ontology terms. Hybrids may more effectively remove toxic metabolites generated during photorespiration and, thus, maintain higher photosynthetic efficiency. These metabolic and proteomic results provide novel insights into heterosis and its utilization for high yielding maize and other crop plants.