Genomics-enabled analysis of specialized metabolism in bioenergy crops: Current progress and challenges

Abstract

Plants produce a staggering diversity of specialized small molecule metabolites that play vital roles in mediating environmental interactions and stress adaptation. This chemical diversity derives from dynamic biosynthetic pathway networks that are often species-specific and operate under tight spatiotemporal and environmental control. A growing divide between demand and environmental challenges in food and bioenergy crop production have intensified research on these complex metabolite networks and their contribution to crop fitness. High-throughput omics technologies provide access to ever-increasing data resources for investigating plant metabolism. However, the efficiency of using such system-wide data to decode the gene and enzyme functions controlling specialized metabolism has remained limited; due largely to the recalcitrance of many plants to genetic approaches and the lack of ‘user-friendly’ biochemical tools for studying the diverse enzyme classes involved in specialized metabolism. With emphasis on terpenoid metabolism in the bioenergy crop switchgrass as an example, this review aims to illustrate current advances and challenges in the application of DNA synthesis and synthetic biology tools for accelerating the functional discovery of genes, enzymes and pathways in plant specialized metabolism. These technologies have accelerated knowledge development on the biosynthesis and physiological roles of diverse metabolite networks across many ecologically and economically important plant species and can provide resources for application to precision breeding and natural product metabolic engineering.

Applications of cell- and tissue-specific ‘omics to improve plant productivity

“…Accordingly, plants produce a plethora of specialised (also known as secondary) metabolites via complex metabolic pathways. These pathways are dynamic and can quickly alter the profile of specialised metabolites thereby enabling plants to adapt and mediate environmental interactions [ 37 , 38 ]. Many specialised metabolites are produced and accumulate to high levels in particular cells or organs that have unique properties ( Figure 2 ) [ 39–41 ].…”

“…The application of individual omics’ technologies in plant research has undoubtedly been very successful, especially in the last decade [ 3–7 , 17 , 38 ]. However, each technology comes with its own technical and data analysis challenges and these are further exacerbated at the single-cell level.…”

Getting back to the grass roots: harnessing specialized metabolites for improved crop stress resilience

“…Tools connecting GRSM to genotypes, reference genomes and pan-genomes are increasingly available for grasses including maize, rice, wheat, sorghum, switchgrass, Miscanthus, Brachypodium distachyon and others [60,61]. While GRSM biosynthetic enzyme classes and gene families can now be partially predicted, specific enzymes of interest often remain unclear.…”

“…Biochemical approaches are commonly used for functional analyses following heterologous protein expression, purification, and in vitro enzymatic assays with chemical substrates when available. Challenges include insufficient protein expression, low enzymatic activity and lack of specialized substrates as pathway intermediates [61]. Improvements in heterologous bacteria and yeast expression platforms are ongoing; however, the predominant tool for GRSM pathway discovery involves use of Nicotiana benthamiana [80].…”

Comparative transcriptomics and metabolomics reveal specialized metabolite drought stress responses in switchgrass (Panicum virgatumL.)

“…In addition, our prior work revealed an expansive network of terpenoid-metabolic terpene synthase ( TPS ) and cytochrome P450 monooxygenase ( P450 ) genes in P. virgatum var. Alamo, and combined metabolite and transcript profiling illustrated the formation of species-specific diterpenoids and the corresponding biosynthetic genes in switchgrass leaves and roots exposed to UV radiation and oxidative stress (Pelot et al 2018; Muchlinski et al 2019; Tiedge et al 2020). Furthermore, emission of volatile mono- and sesqui-terpenoids was observed from switchgrass leaves and roots upon herbivore stress and treatment with defense-related plant hormones (Muchlinski et al 2019).…”