Heat Stress Suppresses Brassica napus Seed Oil Accumulation by Inhibition of Photosynthesis and BnWRI1 Pathway

Abstract

Heat stress during Brassica napus seed filling severely impairs yield and oil content. However, the mechanisms underlying heat-stress effects on B. napus seed photosynthesis and oil accumulation remain elusive. In this study, we showed that heat stress resulted in reduction of seed oil accumulation, whereas the seed sugar content was enhanced, which indicated that incorporation of carbohydrates into triacylglycerols was impaired. Photosynthesis and respiration rates, and the maximum quantum yield of photosystem II in developing seeds were inhibited by heat stress. Transcriptome analysis revealed that heat stress led to up-regulation of genes associated with high light response, providing evidence that photoinhibition was induced by heat stress. BnWRI1 and its downstream genes, including genes involved in de novo fatty acid biosynthesis pathway, were down-regulated by heat stress. Overexpression of BnWRI1 with a seed-specific promoter stabilized both oil accumulation and photosynthesis under the heat-stress condition, which suggested BnWRI1 plays an important role in mediating the effect of heat stress on fatty acid biosynthesis. A number of sugar transporter genes were inhibited by heat stress, resulting in defective integration of carbohydrates into triacylglycerols units. The results collectively demonstrated that disturbances of the seed photosynthesis machinery, impairment of carbohydrates incorporation into triacylglycerols and transcriptional deregulation of the BnWRI1 pathway by heat stress might be the major cause of decreased oil accumulation in the seed.

High temperature patterns during seed maturation determine seed yield and quality in oilseed rape (Brassica napus L.) in relation to sulfur nutrition

“…These results correlate with earlier studies (Aksouhet al 2001;Aksouh-Harradj et al 2006) of intense temperature exposure during seed maturation but contrast with others that highlighted increased total FA contents under a long mild stressing event (Brunel-Muguet et al 2015). Disruption of FA accumulation in OSR has been shown under intense heat stress across a range of temperatures similar to those imposed under our heat-peak conditions, and this was a consequence of photosynthesis inhibition and downregulation of BnWRI1 gene expression, which is a key regulator of FA biosynthesis (Ruuska, Girke, Benning & Ohlrogge 2002;Huang et al 2019). Our results also revealed higher total FA, SFA, and UFA concentrations under LS, but only in specific high-temperature sequences (Figure 2), which contrasted with prior results (Brunel-Muguet et al 2015).…”

“…Other phytohormones were shown to be involved in the control of secondary dormancy, defined as failure in the germination process of mature and non-dormant seeds under adverse conditions (Pekrun, Lutman & Baeumer 1997). Recent studies have highlighted the role of indole-3-acetic acid (IAA), whose concentrations increase in dormancy-induced seeds (Shu, Liu, Xie & He 2016;Liu et al 2019;Tuan, Yamasaki, Kanno, Seo & Ayele 2019). Its high levels have also been correlated with high jasmonic acid (JA) in seeds as a consequence of both phytohormones interacting during the expression of indole glucosinolate biosynthesis genes (Liu et al 2019).…”

“…Recent studies have highlighted the role of indole-3-acetic acid (IAA), whose concentrations increase in dormancy-induced seeds (Shu, Liu, Xie & He 2016;Liu et al 2019;Tuan, Yamasaki, Kanno, Seo & Ayele 2019). Its high levels have also been correlated with high jasmonic acid (JA) in seeds as a consequence of both phytohormones interacting during the expression of indole glucosinolate biosynthesis genes (Liu et al 2019). Although several studies have reported that salicylic acid (SA) enhanced germination in Arabidopsisseeds by reducing oxidative damage (Lee & Park 2010;Chitnis et al 2014), SA has also been shown to inhibit germination because of higher oxidative stress (Xie, Zhang, Hanzlik, Cook & Shen 2007).…”

Effects of long-term high-temperature stress on reproductive growth and seed development in development inBrassica napus

“…High-temperature treatments induce changes in seed oil content and photosynthesis activity. It suggested that the damage to PSII and inhibition of a fatty acid biosynthesis pathway controlled by the transcription factor BnWRI1 might be the major causes of the decreased oil content of B. napus seeds that develop under HS (Huang et al , 2019).…”

DeLTa-Seq: direct-lysate targeted RNA-Seq from crude tissue lysate

“…Quantification of gene expression is a popular approach to study various biological phenomena [1][2][3][4][5][6][7][8] . Recently, large-scale transcriptome analysis by RNA-Seq of hundreds of samples has been emerged in plant biology [9][10][11][12] .…”