Fire and Brimstone: Molecular Interactions between Sulfur and Glucosinolate Biosynthesis in Model and Crop Brassicaceae

Abstract

Glucosinolates (GSLs) represent one of the most widely studied classes of plant secondary metabolite, and have a wide range of biological activities. Their unique properties also affect livestock and human health, and have been harnessed for food and other end-uses. Since GSLs are sulfur (S)-rich there are many lines of evidence suggesting that plant S status plays a key role in determining plant GSL content. However, there is still a need to establish a detailed knowledge of the distribution and remobilization of S and GSLs throughout the development of Brassica crops, and to represent this in terms of primary and secondary sources and sinks. The increased genome complexity, gene duplication and divergence within brassicas, together with their ontogenetic plasticity during crop development, appear to have a marked effect on the regulation of S and GSLs. Here, we review the current understanding of inorganic S (sulfate) assimilation into organic S forms, including GSLs and their precursors, the intracellular and inter-organ transport of inorganic and organic S forms, and the accumulation of GSLs in specific tissues. We present this in the context of overlapping sources and sinks, transport processes, signaling molecules and their associated molecular interactions. Our analysis builds on recent insights into the molecular regulation of sulfate uptake and transport by different transporters, transcription factors and miRNAs, and the role that these may play in GSL biosynthesis. We develop a provisional model describing the key processes that could be targeted in crop breeding programs focused on modifying GSL content.

Dissection of the genetic architecture of three seed‐quality traits and consequences for breeding in Brassica napus

“…However, it was found that the number of associated loci for GSC is much higher than that for EAC, which is consistent with a more complex genetic architecture for GSC compared with EAC (Review in introduction). This is likely to be due to the influence of multiple factors affecting total seed GSC, including the biosynthesis of aliphatic, benzenic and indolic glucosinolates, and the breakdown and transportation of glucosinolates (Borpatragohain et al ., ; Nour‐Eldin et al ., ; Wittstock and Burow, ), which was also supported by the candidate genes identified in this study (Figures and S5). In contrast, erucic acid is a single compound, which is extended from a single well‐defined substrate (oleic acid) by FAE1.…”

“…Using this approach, we identified additional novel candidate genes associated with GSC and SOC. For GSC, the annotation of 27 putative candidate genes at fifteen associated loci implicated roles not only in the biosynthesis of aliphatic, benzenic and indolic glucosinolates, but also in the breakdown and transportation of glucosinolates (Table S6) (Borpatragohain et al ., ; Nour‐Eldin et al ., ; Wittstock and Burow, ). Association analysis between functional variations in gene regions and GSC variation revealed that seed GSC was highly correlated with four genes including BnaA9.APK1 , BnaA5.NSP1 , BnaA6.MYB118 and BnaA9.AOP3 (Figures and S5).…”

Understanding of MYB Transcription Factors Involved in Glucosinolate Biosynthesis in Brassicaceae

“…A genome-wide comparison of genes related to GSL biosynthesis suggested that genome duplication resulted in the expansion of GSLs-related genes in the Brassica genome [ 10 , 14 , 15 ]. Furthermore, functional analysis of these genes has demonstrated that GSL biosynthesis in Brassica species is controlled by more regulators than in Arabidopsis , because of their polyploid genomes [ 16 , 17 ]. This indicates that GSL biosynthesis of Brassica species has a regulatory network distinct from Arabidopsis .…”

“…Recently, some MYB TFs were described as the regulatory factors directly or indirectly activating GSL pathway genes [ 18 , 19 , 20 ]. Studies have used various molecular biological approaches to investigate GSL biosynthesis in A. thaliana and Brassica species [ 16 , 17 , 18 ]. Some R2R3 MYB transcription factors (TFs) with two MYB repeats (R2R3) control GSL biosynthesis.…”

Comprehensive Transcriptomic Analysis for Developing Seeds of a Synthetic Brassica Hexaploid

“…Transcription factors, as a kind of important regulatory factors, play an important role in the growth and development of plants. Transcription factors (TFs) also have an important impact on the adaptability of polyploids, such as influencing the morphology of polyploid rapeseed [ 15 ], the expression of non-additive genes in polyploid Arabidopsis thaliana [ 16 ] and the biosynthesis of GSL in polyploid Brassica species [ 17 , 18 ].…”