Both Biosynthesis and Transport Are Involved in Glucosinolate Accumulation During Root-Herbivory in Brassica rapa

Abstract

The optimal defense theory predicts that plants invest most energy in those tissues that have the highest value, but are most vulnerable to attacks. In Brassica species, root-herbivory leads to the accumulation of glucosinolates (GSLs) in the taproot, the most valuable belowground plant organ. Accumulation of GSLs can result from local biosynthesis in response to herbivory. In addition, transport from distal tissues by specialized GSL transporter proteins can play a role as well. GSL biosynthesis and transport are both inducible, but the role these processes play in GSL accumulation during root-herbivory is not yet clear. To address this issue, we performed two time-series experiments to study the dynamics of transport and biosynthesis in local and distal tissues of Brassica rapa. We exposed roots of B. rapa to herbivory by the specialist root herbivore Delia radicum for 7 days. During this period, we sampled above-and belowground plant organs 12 h, 24 h, 3 days and 7 days after the start of herbivory. Next, we measured the quantity and composition of GSL profiles together with the expression of genes involved in GSL biosynthesis and transport. We found that both benzyl and indole GSLs accumulate in the taproot during root-herbivory, whereas we did not observe any changes in aliphatic GSL levels. The rise in indole GSL levels coincided with increased local expression of biosynthesis and transporter genes, which suggest that both biosynthesis and GSL transport play a role in the accumulation of GSLs during root herbivory. However, we did not observe a decrease in GSL levels in distal tissues. We therefore hypothesize that GSL transporters help to retain GSLs in the taproot during root-herbivory.

Unravelling Plant Responses to Stress—The Importance of Targeted and Untargeted Metabolomics

“…Dependent upon the host plant species under investigation, as well as the nature of the biotic stress (and in some examples, abiotic stress), a range of plant secondary metabolite classes, with known toxicity against microbes and/or insects, are present and should be considered for analysis. Classically, glucosinolates and isothiocyanates are important defensive compounds in Brassica responses to herbivory [ 31 , 61 ], as are alkaloids in a range of species, especially the Solanaceae [ 62 , 63 ] and benzoxazinoids, for example DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one) in cereals such as maize [ 64 ]. With respect to both microbial pathogens and insect herbivores, phenolic compounds, such as the cyanogenic glycosides [ 65 , 66 , 67 ], flavonoids [ 68 , 69 , 70 ], and lignins [ 71 , 72 ], play important roles, as do carotenoids, in relation to stress response signaling and abiotic stress [ 73 ], and terpenes, which serve as volatile stress signals that prime neighboring leaves and plants [ 74 , 75 ].…”

Plant Secondary Metabolite Transporters: Diversity, Functionality, and Their Modulation

“…However, the exact transportation mechanism still needs more experimental validation (Jiang et al, 2019). Similarly, in the recent past, the probable role of GTRs in the allocation of GSLs has also been deciphered in response to root herbivory in Brassica rapa, which suggested the involvement of two transporter genes namely GTR1 and GTR2 (Touw et al, 2020). The indole and benzyl GSLs were found to be highly accumulated in the taproot of B. rapa during the attack of Delia radicum, which is possibly due to their increased biosynthesis and/or transport from distal organs.…”

“…At the same time, GSL transporter and biosynthesis genes were also upregulated, which implies their role in the transport of GSLs from distal organs and/or enhanced biosynthesis in the taproot. Despite the increased expression of GTR genes in taproot, there was no reduction in the GSL concentration in distal tissues such as shoot but authors still hypothesized that these transporters are somehow involved in the retention of GSLs in taproot to fulfill the immediate requirement for combating the pathogen attack, although the precise molecular mechanism remained unclear ( Touw et al, 2020 ).…”

“…Whereas the significance of ethylene in regulating the activity of AtABCG40 transporter was observed when pathogen-induced expression of AtABCG40 transporter was significantly upregulated to 16-fold at 3 h after being treated with ethylene ( Campbell et al, 2003 ). Moreover, the role of biotic stresses in transporter regulation is also evidently highlighted by significant upregulation of the glucosinolate transporters GTR1 and GTR2 of B. rapa in response to herbivory ( Touw et al, 2020 ). Likewise, expression of NpPDR1 is also found to be induced following infection with fungal ( Botrytis cinerea ) and bacterial ( Pseudomonas syringae ) pathogens via JA signaling pathway ( Stukkens et al, 2005 ).…”

Human, Animal and Plant Health Benefits of Glucosinolates and Strategies for Enhanced Bioactivity: A Systematic Review

“…Managing plants using chemicals and light may increase GSs content, for instance 6-benzylaminopurine [ 175 ] alone and in combination with 1-methyl-cyclopropene [ 176 ] increases GSs in broccoli and green light emitting diode lights increase broccoli’s florets’ total GSs content and sulforaphane [ 177 ]. Elsewhere, GSs in plants may accumulate through natural occurrences, in response various stresses like yearly seasonal variations that cause increased temperatures, water stress [ 168 ], larval/herbivore infestation [ 166 , 178 , 179 ], ozone fumigation [ 180 ], and biotechnological transformations [ 172 , 181 ].…”