A Novel Chimeric Mitochondrial Gene Confers Cytoplasmic Effects on Seed Oil Content in Polyploid Rapeseed (Brassica napus)

Abstract

Cytoplasmic effects (CEs) have been discovered to influence a diverse array of agronomic traits in crops, and understanding the underlying mechanisms can help accelerate breeding programs. Seed oil content (SOC) is of great agricultural, nutritional, and economic importance. However, the genetic basis of CEs on SOC (CE-SOC) remains enigmatic. In this study, we use an optimized approach to sequence the cytoplasmic (plastid and mitochondrial) genomes of allotetraploid oilseed rape (Brassica napus) cultivars, 51218 and 56366, that bear contrasting CE-SOC. By combining comparative genomics and genome-wide transcriptome analysis, we identify mitochondria-encoded orf188 as a potential CE-SOC determinant gene. Functional analyses in the model system Arabidopsis thaliana and rapeseed demonstrated that orf188 governs CE-SOC and could significantly increase SOC, strikingly, through promoting the yield of ATP. Consistent with this finding, transcriptional profiling with microarray and RNA sequencing revealed that orf188 affects transcriptional reprogramming of mitochondrial energy metabolism to facilitate ATP production. Intriguingly, orf188 is a previously uncharacterized chimeric gene, and the presence of this genetic novelty endows rapeseed with positive CE-SOC. Our results shed light on the molecular basis of CEs on a key quantitative trait in polyploid crops and enrich the theory of maternal control of oil content, providing new scientific guidance for breeding high-oil rapeseed germplasms.

Nonspecific phospholipase C6 increases seed oil production in oilseed Brassicaceae plants

“…As demonstrated in various plants through forward genetics, the effect of identified loci controlling SOC was < 1–2% in Arabidopsis (Hobbs et al , 2004; Branham et al , 2015), soybean (Hwang et al , 2014; Zhou et al , 2015), maize (H. Li et al , 2013), and oilseed rape (Li et al , 2014; Liu et al , 2016). A 1% increase in SOC is equivalent to a 2.5–3% increase in oilseed rape yield (Liu et al , 2016, 2019). It was shown previously that the trait of SOC was controlled primarily by additive effect and thus gene‐pyramiding breeding is often used to improve the SOC (H. Li et al , 2013; Liu et al , 2016).…”

The Use of Genetic and Gene Technologies in Shaping Modern Rapeseed Cultivars (Brassica napus L.)

“…The roles of LPAAT genes of B. napus , BnLPAT2 and BnLPAT5, in regulating oil biosynthesis has been recently confirmed by targeted mutations using Cas9 with single-gRNAs and multi-sgRNAs whereby the resulted Bnlat2 and Bnlat5 mutants showed decreased oil content and enlarged oil bodies [ 33 ]. Cytoplasmic genomes are also attracting more interest as the new approach for maximizing oil content in canola [ 90 ].…”

Comparison of the cytoplastic genomes by resequencing: insights into the genetic diversity and the phylogeny of the agriculturally important genus Brassica

“…The chloroplast and mitochondrial genome sequences of a B. napus strain 51218 [22], which is an intermediate breeding material of nap mitotype, were respectively used as reference sequences to call the overall cpDNA and mtDNA basic variants. The calling was conducted by standard BWA/Genome Analysis Toolkit (GATK) pipeline with manual inspection [30], and then randomly veri ed by Kompetitive Allele Speci c PCR (KASP) analysis.…”

“…Previous cpDNA and mtDNA-based studies were separated and never been corresponded and integrated to accurately explore the multiply origin of B. napus. Cytoplasmic DNA and its corresponding cytonuclear interactions, are highly valuable for crop breeding not only due to its cause of cytoplasmic male sterility [21], but also in the association with certain agricultural traits, e.g., high seed-oil content in nap-type rapeseed [22] and plant resistance to adverse living environment. Here in this study, a well-chosen set of plant materials centering on B. napus have been synchronously resequenced at the cpDNA and mtDNA level, a systematic genetic investigation and an elaborate phylogenetic pedigree at intraspeci c level have been constructed, with the purpose of improving our understanding of the whole Brassica genus.…”