Uncovering Pathways Highly Correlated to NUE through a Combined Metabolomics and Transcriptomics Approach in Eggplant.

Antonio Mauceri,Francesco Sunseri,Laura Toppino,Francesco Mercati,Maria Rosa Abenavoli,Antonio Lupini,Fabrizio Araniti,Asaph Aharoni,Meriem Miyassa Aci,Maria Rosaria Panuccio,Sayantan Panda,Sagit Meir,Giuseppe Leonardo Rotino

doi:10.3390/plants11050700

Abstract

Nitrogen (N) fertilization is one of the main inputs to increase crop yield and food production. However, crops utilize only 30–40% of N applied; the remainder is leached into the soil, causing environmental and health damage. In this scenario, the improvement of nitrogen-use efficiency (NUE) will be an essential strategy for sustainable agriculture. Here, we compared two pairs of NUE-contrasting eggplant (Solanum melongena L.) genotypes, employing GC-MS and UPLC-qTOF-MS-based technologies to determine the differential profiles of primary and secondary metabolites in root and shoot tissues, under N starvation as well as at short- and long-term N-limiting resupply. Firstly, differences in the primary metabolism pathways of shoots related to alanine, aspartate and glutamate; starch, sucrose and glycine; serine and threonine; and in secondary metabolites biosynthesis were detected. An integrated analysis between differentially accumulated metabolites and expressed transcripts highlighted a key role of glycine accumulation and the related glyA transcript in the N-use-efficient genotypes to cope with N-limiting stress. Interestingly, a correlation between both sucrose synthase (SUS)- and fructokinase (scrK)-transcript abundances, as well as D-glucose and D-fructose accumulation, appeared useful to distinguish the N-use-efficient genotypes. Furthermore, increased levels of L-aspartate and L-asparagine in the N-use-efficient genotypes at short-term low-N exposure were detected. Granule-bound starch synthase (WAXY) and endoglucanase (E3.2.1.4) downregulation at long-term N stress was observed. Therefore, genes and metabolites related to these pathways could be exploited to improve NUE in eggplant.

Highlights

Soil-N availability is one of the most important factors limiting worldwide plant growth and productivity
Root and shoot extracts derived from high (AM222 and 67-3)- and low (305E40 and AM22)-NUE eggplant genotypes were profiled using Gas Chromatography–Mass Spectrometry (GC-MS) and high-resolution MS (HRMS; UPLC-qTOF-MS; mainly secondary, semipolar metabolites) to examine the plant response to N starvation as well as short- and long-term N-limited resupply
In HRMS analysis, we focused on nitrogen-containing metabolites, mainly glycoalkaloids (Supplementary Table S1B)

Summary

Introduction

Soil-N availability is one of the most important factors limiting worldwide plant growth and productivity. Nitrogen limitation leads to many functional damages, inducing alterations in physiological, biochemical, and molecular processes such as photosynthesis, respiration, ion uptake and translocation, carbon metabolism, and senescence [1,2]. Excessive use of N determines negative effects on the environment, economy, and human health [4]. Nitrogen-use-efficiency (NUE) improvement in crop plants, together with low-N-fertilizer input and best-management practices, could represent strategies to limit the negative impact of agriculture on the environment and human health [5]. NUE, defined as “the grain yield per unit of N available in the soil”, is a complex trait under physiological, biochemical, and genetic control [6,7]. Efforts have been made to identify molecular mechanisms underlying NUE to improve this complex trait by conventional breeding programs in several crops [8]. Metabolomics, transcriptomics, and proteomics are becoming valuable tools in model and crop species to understand changes in biological processes, genes, and chemical composition of primary and secondary metabolites involved in stress responses, including N deficiency [9–11]

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Discussion

Conclusion