Biochemical Genetics of Metabolic Plasticity

Background: Soil salinization represents a critical global challenge to agricultural productivity, profoundly impacting crop yields and threatening food security. Plant salt-responsive is complex and dynamic, making it challenging to fully elucidate salt tolerance mechanism and leading to gaps in our understanding of how plants adapt to and mitigate salt stress. Results: Here, we conduct high-resolution time-series transcriptomic and metabolomic profiling of the extremely salt-tolerant maize inbred line, HLZY, and the salt-sensitive elite line, JI853. Utilizing advanced data mining techniques, we identify key factors underlying the divergence in salt tolerance between these two lines and discover a series of novel genes and metabolites essential for maize salt tolerance. Additionally, we develop an innovative decision algorithm that enabled the construction of a high-confidence gene regulatory network for important salt-responsive metabolites. Comprehensive genetic and molecular studies further reveal the pivotal role of a hub gene, ZmGLN2, in regulating metabolite biosynthesis and salt tolerance in maize. Conclusions: Our study provides the first high-resolution transcriptomic and metabolomic dataset for crop salt response, uncovering novel maize salt-responsive genes and metabolites. These findings demonstrate the effectiveness of high-resolution multi-omics in deciphering the mechanisms underlying complex crop traits. Furthermore, we develop a systematic analytical framework for mining time-series multi-omics data, which can be broadly applied to other species or traits.

In recent years, several studies investigating multifactorial stresses have emerged. This shift has been driven by the recognition that one of the primary reasons for the inconsistency between laboratory-based results and field observations of plant responses is that, in natural environments, plants are routinely exposed to a combination of biotic and/or abiotic stresses, which they encounter either simultaneously or sequentially. Within this review, we address current advances in multifactorial studies focusing on metabol(om)ic changes in model as well as cereal crop species. The common consensus is that currently, studies on phenotypic and transcriptomics analysis are prevailing, while metabolic studies are scarce. Despite the need for further studies to validate the findings in this review, two clear biological messages emerge. First, and perhaps unsurprisingly, proline stands out as a universal stress metabolite, closely followed by branched-chain amino acids. Interestingly, while multifactorial stress responses are often considered non-additive and unpredictable, our findings reveal that many metabolic changes are both. Expanding the scope of studies to include more species and a wider range of stresses at the metabolic level will be essential for uncovering additional metabolic reprogramming in response to multifactorial stress. This will provide invaluable insights for developing breeding strategies aimed at future-proofing crops.

Sulfur (S) metabolism has played a critical role in the evolution of life, serving as an energy source for early biochemical pathways like dissimilatory S reduction and anoxygenic photosynthesis. Across kingdoms, S metabolism displays remarkable diversity. S-containing metabolites like glucosinolates (GLSs) in Brassicaceae and S-alk(en)ylcysteine sulfoxides in Allium species illustrate the ecological and evolutionary significance of Scontaining compounds. These metabolites contribute to defense, homeostasis, and ecological interactions, with mechanisms like enzymatic hydrolysis releasing bioactive molecules such as allicin. Further, advances in transcriptomics and biochemical studies have revealed the genetic underpinnings of S metabolism and specialized pathways in bulb-forming Allium species. The role extends to ecological interactions by modulating S-associated defense pathways. This integrative understanding of S metabolism underscores its evolutionary, physiological, and ecological importance.

Metabolomics, a rapidly evolving field, has revolutionized horticultural crop research by enabling comprehensive analysis of metabolites that influence plant yield, growth, quality and nutritional value. The integration of web-based resources, including databases, computational tools and analytical platforms has significantly enhanced metabolomics studies by facilitating data processing, metabolite identification and pathway analysis. Moreover, the application of machine learning algorithms to these web resources has further optimized data interpretation, enabling more accurate prediction of metabolic profiles. Publicly available reference libraries and bioinformatic tools support precision of breeding, postharvest quality assessment and ultimately improving crop yield and sustainability. In this mini-review, we explore the current status of the diverse range of plant metabolomics databases in horticultural crops, highlighting the synergy between machine learning and traditional bioinformatics methods, their applications, challenges and future prospects in advancing plant science and agricultural innovation.

Metabolomics is a rapidly evolving field focused on the comprehensive identification and quantification of small molecules in biological systems. As the final layer of the biological hierarchy following of the genome, transcriptome and proteome, it presents a dynamic snapshot of phenotype, influenced by genetic, environmental and physiological factors. Whilst the metabolome sits downstream of genes and proteins, there are multiple higher levels—tissues, organs, the entire organism, and interactions with other organisms, which need to be considered in order to fully comprehend organismal biology. Advances in metabolomics continue to expand its applications in plant biology, biotechnology, and natural product discovery unlocking many of nature’s most beneficial colors, tastes, nutrients and medicines. Flavonoids and other specialized metabolites are essential for plant defense against oxidative stress and function as key phytonutrients for human health. Recent advancements in gene-editing and metabolic engineering have significantly improved the nutritional value and flavor of crop plants. Here we highlight how advanced metabolic analysis is driving improvements in crops uncovering genes that influence nutrient and flavor profile and plant derived compounds with me-dicinal potential.

In a recent study, Satterlee et al. found that the repeated emergence of prickleless varieties in Solanaceae species is a convergent trait caused by loss of function in the cytokinin-activating enzyme LONELY GUY (LOG). New prickleless forms can be created in wild and domesticated forms using gene editing.

0

Plant metabolism is profoundly affected by various abiotic stresses. Consequently, plants must reconfigure their metabolic networks to sustain homeostasis while synthesizing compounds that mitigate stress. This aspect, with the current intensified climate impact results in more frequent abiotic stresses on a global scale. Advances in metabolomics and systems biology in past decades have enabled both a comprehensive overview and a detailed analysis of key components involved in the plant metabolic response to abiotic stresses. This review addresses metabolic responses to altered atmospheric CO2 and O3, water deficit, temperature extremes, light intensity fluctuations including the importance of UV-B, ionic imbalance, and oxidative stress predicted to be caused by climate change, long-term shifts in temperatures, and weather patterns. It also assesses both the commonalities and specificities of metabolic responses to diverse abiotic stresses, drawing on data from the literature. Classical stress-related metabolites such as proline, and polyamines are revisited, with an emphasis on the critical role of branched-chain amino acid metabolism under stress conditions. Finally, where possible, mechanistic insights into the regulation of metabolic processes and further outlook on combinatory stresses are discussed.

0

Capsicum (pepper) is among the most economically important species worldwide, and its fruits accumulate specialized metabolites with essential roles in plant environmental interaction and human health benefits as well as in conferring their unique taste. However, the genetics underlying differences in metabolite presence/absence and/or accumulation remain largely unknown. In this study, we carried out a genome-wide association study as well as generating and characterizing a novel backcross inbred line mapping population to determine the genetic architecture of the pepper metabolome. This genetic analysis provided over 1,000 metabolic quantitative trait loci (mQTL) for over 250 annotated metabolites. We identified 92 candidate genes involved in various mQTLs. Among the identified loci, we described and validated a gene cluster of eleven UDP-glycosyltransferases (UGTs) involved in monomeric capsianoside biosynthesis. We additionally constructed the gene-by-gene-based biosynthetic pathway of pepper capsianoside biosynthesis, including both core and decorative reactions. Given that one of these decorative pathways, namely the glycosylation of acyclic diterpenoid glycosides, contributes to plant resistance, these data provide new insights and breeding resources for pepper. They additionally provide a blueprint for the better understanding of the biosynthesis of species-specific natural compounds in general.