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

Abstract

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.

A seed‐like proteome in oil‐rich tubers

“…We additionally compared the expression levels of the genes coding for the tuber‐specific proteins by investigating the recently published transcriptomes of yellow nutsedge and the respective homologs in purple nutsedge (Ji et al., 2021; Figure 2b) In this study, tubers were harvested 20, 50, and 90 days after tuber formation. All of the seven ‘seed’ protein‐coding genes had at least 10 times higher transcript levels in yellow nutsedge than in purple nutsedge when averaging the three tuber stages per species analyzed in the study (taking also into account transcripts with very high similarity; Data S5).…”

“…There are striking similarities between Arabidopsis seeds and tubers of yellow but not purple nutsedge. It is therefore conceivable that oil accumulation and desiccation tolerance of both organs are based on a similar proteome and the underlying gene expression pattern that could be regulated by a similar network of hormones and transcription factors, as for example the transcription factors ABSCISIC ACID INSENSITIVE3 (ABI3), WRINKLED1 (WRI1), and LEAFY COTYLEDON1 (LEC1), which show increased expression levels in the tubers of yellow nutsedge in comparison to purple nutsedge (Figure S7; Ji et al., 2021).…”

“…In addition, RNA‐seq data of purple nutsedge tubers (Ji et al., 2021) were downloaded from NCBI (SRA) and coding sequences were predicted using TransDecoder v.5.5.0 with default settings.…”

“…Given are log 2 -transformed & riBAQ values. (b) Expression of homologous proteins identified in transcriptomes of yellow and purple nutsedge based on previously published data (Ji et al, 2021; closely related homologs were accounted for). Given are log 2transformed TMM values.…”

Crystal structure of Arabidopsis thaliana HPPK/DHPS, a bifunctional enzyme and target of the herbicide asulam

“…Sequence alignments and analysis HPPK/DHPS sequences were retrieved from NCBI Protein BLAST using A. thaliana mitHPPK/DHPS as the query. Transcriptomes of weed species commonly targeted by asulam in the field were assembled using CLC Genomics Workbench v20.0.3 (Qiagen Aarhus A/S) from data in the NCBI Sequence Read Archive: L. multiflorum (accession SRR1648407) (Czaban et al, 2015), E. crus-galli (SRR8633067) (Fang et al, 2019), C. rotundus (SRR12887711) (Ji et al, 2021) and P. annua (SRR1633980) (Chen et al, 2016). Protein sequences of HPPK-DHPS from these species were obtained using tBLASTn by searching the transcriptomes against the A. thaliana mitHPPK/DHPS protein sequence.…”