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Multiomics of a rice population identifies genes and genomic regions that bestow low glycemic index and high protein content
Sunday, 2024/09/08 | 07:10:10
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Saurabh Badoni, Erstelle A Pasion-Uy, Sakshi Kor, Sung-Ryul Kim, Rhowell N Tiozon Jr, Gopal Misra, Reuben James Q Buenafe, Luster May Labarga, Ana Rose Ramos-Castrosanto, Vipin Pratap, Inez Slamet-Loedin, Julia von Steimker, Saleh Alseekh, Alisdair R Fernie, Ajay Kohli, Gurudev S Khush, Nese Sreenivasulu PNAS; 2024 Sep 3; 121(36):e2410598121. doi:10.1073/pnas.2410598121. SignificanceIn line with intensified efforts to combat the multifaceted impacts of malnutrition, there is a pressing need to develop diabetic-friendly, healthier rice varieties to tackle the escalating global prevalence of diabetes. In this study, we developed recombinant inbred lines with milled rice exhibiting ultralow to low glycemic index (GI) and high protein content (PC) from the cross between Samba Mahsuri and IR36 amylose extender. We performed comprehensive genomics and metabolomics complemented with modeling analyses emphasizing the importance of OsSBEIIb along with additional candidate genes whose variations allowed us to produce target rice lines with lower GI and high PC in a high-yielding background. These lines represent an important breeding resource to address food and nutritional security. AbstractTo counter the rising incidence of diabetes and to meet the daily protein needs, we created low glycemic index (GI) rice varieties with protein content (PC) surpassing 14%. In the development of recombinant inbred lines using Samba Mahsuri and IR36 amylose extender (IR36ae) as parental lines, we identified quantitative trait loci and genes associated with low GI, high amylose content (AC), and high PC. By integrating genetic techniques with classification models, this comprehensive approach identified candidate genes on chromosome 2 (qGI2.1/qAC2.1 spanning the region from 18.62 Mb to 19.95 Mb), exerting influence on low GI and high amylose. Notably, the phenotypic variant with high value was associated with the recessive allele of the starch branching enzyme 2b (sbeIIb). The genome-edited sbeIIb line confirmed low GI phenotype in milled rice grains. Further, combinations of alleles created by the highly significant SNPs from the targeted associations and epistatically interacting genes showed ultralow GI phenotypes with high amylose and high protein. Metabolomics analysis of rice with varying AC, PC, and GI revealed that the superior lines of high AC and PC, and low GI were preferentially enriched in glycolytic and amino acid metabolisms, whereas the inferior lines of low AC and PC and high GI were enriched with fatty acid metabolism. The high amylose high protein recombinant inbred line (HAHP_101) was enriched in essential amino acids like lysine. Such lines may be highly relevant for food product development to address diabetes and malnutrition.
Figure 3: Metabolomic analysis of HAHP and LALP groups. (A) Hierarchical clustering using 275 metabolites distinguished the HAHP (top red bar: UM_10, UM_3, UM_4) and LALP (top green bar: UM_9, UM_1, UM_2) samples. The red and green colors in the heatmap represent HAHP and LALP, respectively. (B) Pathway enrichment analysis comparing HAHP and LALP groups showed significant (P < 0.05, pathway impact > 0.1) differences in amino acid–related pathways (i.e., metabolism of Cys, Met, Val, Leu, Ile, Trp, Ala, Asp, Glu, and glutathione) and fatty acid-related pathways (i.e., linoleic acid metabolism, cutin, suberin, and wax biosynthesis). The size of the node representing each enriched pathway is directly proportional to the enrichment ratio (number of observed divided by the number of expected metabolites in a pathway), while the color intensity of the node depicts the P-value with lower values for darker orange color. (C) Top 25 types of metabolites identified from the significantly enriched pathways comparing the HAHP and LALP groups. Similarly, the size and color of the nodes represent the enrichment ratio and P-values, respectively. (D) Top four specific metabolites (P < 0.003) accumulating in the HAHP group based on mass-to-charge ratio over retention time analysis. Each dot in pink color represents a specific metabolite passing the significance threshold −log10(p) > 1.0. Boxplots comparing HAHP and LALP for these top four specific metabolites are shown above the dotplot with pairwise comparisons based on the t test. (E) Isolated protein concentrate from the milled grains of the HAHP line (HAHP_101) showed higher protein yield compared to the parental Samba Mahsuri. (F) Rice protein powder from the HAHP_101 exhibited higher levels of various EAAs compared to the parental Samba Mahsuri. |
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