An Expanded Role for WRINKLED1 Metabolic Control Based on Combined Phylogenetic and Biochemical Analyses

2020

Preprint

Yellow nutsedge is a specific plant species that contains significant amounts of both starch and oil as the main reserves in storage tuber. Its tuber can accumulate up to 35% oil of dry weight, perhaps the highest level observed in the tuber tissues of plant kingdom. To gain insight into the molecular mechanism that leads to high oil accumulation in yellow nutsedge, gene expression profiles of oil production pathways involved carbon metabolism, fatty acid synthesis, triacylglycerol synthesis, and triacylglycerol storage during tuber development were compared with purple nutsedge, a very close relative of yellow nutsedge that is poor in oil accumulation. Compared with purple nutsedge, the high oil content in yellow nutsedge was associated with much higher transcripts for seed-like oil-body proteins, almost all fatty acid synthesis enzymes, and specific key enzymes of plastid Rubisco bypass as well as malate and pyruvate metabolism. However, transcript levels for carbon metabolism toward pyruvate generation were comparable and for triacylglycerol synthesis were similar in both species. Two seed-like master transcription factors ABI3 and WRI1 were found to display similar temporal transcript patterns but be expressed at 6.5- and 14.3-fold higher levels in yellow nutsedge than in purple nutsedge, respectively. A weighted gene co-expression network analysis revealed that ABI3 is in strong transcriptional coordination with WRI1 and other key oil-related genes. Together, these results implied that plastidial pyruvate availability and fatty acid synthesis, along with triacylglycerol storage in oil body, rather than triacylglycerol synthesis in endoplasmic reticulum, are the major factors responsible for high oil production in tuber of yellow nutsedge, and ABI3 is most likely to play a critical role in regulating oil accumulation. This study will aid understanding in underlying molecular mechanism controlling carbon partitioning toward oil production in oil-rich tuber and provide valuable reference for enhancing oil accumulation in non-seed tissues of crops through genetic breeding or metabolic engineering.

Section: Resultssupporting

confidence: 92%

High oil accumulation in tuber of yellow nutsedge compared to purple nutsedge is associated with more abundant expression of genes involved in fatty acid synthesis and triacylglycerol storage

2020

Preprint

“…10 a; Additional file 1 : Table S4). Our analysis result of WRI1 in concerted regulation with the genes related to carbon metabolism, fatty acid synthesis, and TAG synthesis in yellow nutsedge tuber is similar to recent reports [ 66 , 67 ]. These oil-related target genes are co-regulated by both of ABI3 and WRI1 , indicating an overlapping set of targets for the two transcription factors.…”

Section: Resultssupporting

confidence: 91%

High oil accumulation in tuber of yellow nutsedge compared to purple nutsedge is associated with more abundant expression of genes involved in fatty acid synthesis and triacylglycerol storage

2021

Biotechnol Biofuels

Background Yellow nutsedge is a unique plant species that can accumulate up to 35% oil of tuber dry weight, perhaps the highest level observed in the tuber tissues of plant kingdom. To gain insight into the molecular mechanism that leads to high oil accumulation in yellow nutsedge, gene expression profiles of oil production pathways involved carbon metabolism, fatty acid synthesis, triacylglycerol synthesis, and triacylglycerol storage during tuber development were compared with purple nutsedge, the closest relative of yellow nutsedge that is poor in oil accumulation. Results Compared with purple nutsedge, high oil accumulation in yellow nutsedge was associated with significant up-regulation of specific key enzymes of plastidial RubisCO bypass as well as malate and pyruvate metabolism, almost all fatty acid synthesis enzymes, and seed-like oil-body proteins. However, overall transcripts for carbon metabolism toward carbon precursor for fatty acid synthesis were comparable and for triacylglycerol synthesis were similar in both species. Two seed-like master transcription factors ABI3 and WRI1 were found to display similar transcript patterns but were expressed at 6.5- and 14.3-fold higher levels in yellow nutsedge than in purple nutsedge, respectively. A weighted gene co-expression network analysis revealed that ABI3 was in strong transcriptional coordination with WRI1 and other key oil-related genes. Conclusions These results implied that pyruvate availability and fatty acid synthesis in plastid, along with triacylglycerol storage in oil bodies, rather than triacylglycerol synthesis in endoplasmic reticulum, are the major factors responsible for high oil production in tuber of yellow nutsedge, and ABI3 most likely plays a critical role in regulating oil accumulation. This study is of significance with regard to understanding the molecular mechanism controlling carbon partitioning toward oil production in oil-rich tuber and provides a valuable reference for enhancing oil accumulation in non-seed tissues of crops through genetic breeding or metabolic engineering.

“…10A; Additional le 1: Table S4). Our analysis result of WRI1 in concerted regulation with the genes related to carbon metabolism, fatty acid synthesis, and TAG synthesis in yellow nutsedge tuber is similar to recent reports [66,67]. These oil-related target genes are co-regulated by both of ABI3 and WRI1, indicating an overlapping set of targets for the two transcription factors.…”

Section: Great Transcriptional Divergence Of Tag Storage Genes Betweesupporting

confidence: 89%

High oil accumulation in tuber of yellow nutsedge compared to purple nutsedge is associated with more abundant expression of genes involved in fatty acid synthesis and triacylglycerol storage

2021

Preprint

Background: Yellow nutsedge is a unique plant species that can accumulate up to 35% oil of tuber dry weight, perhaps the highest level observed in the tuber tissues of plant kingdom. To gain insight into the molecular mechanism that leads to high oil accumulation in yellow nutsedge, gene expression profiles of oil production pathways involved carbon metabolism, fatty acid synthesis, triacylglycerol synthesis, and triacylglycerol storage during tuber development were compared with purple nutsedge, the closest relative of yellow nutsedge that is poor in oil accumulation. Results: Compared with purple nutsedge, high oil accumulation in yellow nutsedge was associated with significant up-regulation of specific key enzymes of plastidial Rubisco bypass as well as malate and pyruvate metabolism, almost all fatty acid synthesis enzymes, and seed-like oil-body proteins. However, overall transcripts for carbon metabolism toward carbon precursor for fatty acid synthesis were comparable and for triacylglycerol synthesis were similar in both species. Two seed-like master transcription factors ABI3 and WRI1 were found to display similar transcript patterns but were expressed at 6.5- and 14.3-fold higher levels in yellow nutsedge than in purple nutsedge, respectively. A weighted gene co-expression network analysis revealed that ABI3 was in strong transcriptional coordination with WRI1 and other key oil-related genes. Conclusions: These results implied that pyruvate availability and fatty acid synthesis in plastid, along with triacylglycerol storage in oil bodies, rather than triacylglycerol synthesis in endoplasmic reticulum, are the major factors responsible for high oil production in tuber of yellow nutsedge, and ABI3 most likely plays a critical role in regulating oil accumulation. This study is of significance with regard to understanding the molecular mechanism controlling carbon partitioning toward oil production in oil-rich tuber and provides a valuable reference for enhancing oil accumulation in non-seed tissues of crops through genetic breeding or metabolic engineering.