Integrative Transcriptomic and Metabolomic Analysis at Organ Scale Reveals Gene Modules Involved in the Responses to Suboptimal Nitrogen Supply in Tomato

Begoña Renau-Morata,Joaquín Cañizares,Eugenio G Minguet,Eva Jiménez-Benavente,Jaime Cebolla-Cornejo,Joaquín Medina,Lu Yang,Rosa-Victoria Molina,Sergio G Nebauer,Laura Carrillo,Víctor García-Carpintero,Raúl Martí,Javier Canales

doi:10.3390/agronomy11071320

Abstract

The development of high nitrogen use efficiency (NUE) cultivars under low N inputs is required for sustainable agriculture. To this end, in this study, we analyzed the impact of long-term suboptimal N conditions on the metabolome and transcriptome of tomato to identify specific molecular processes and regulators at the organ scale. Physiological and metabolic analysis revealed specific responses to maintain glutamate, asparagine, and sucrose synthesis in leaves for partition to sustain growth, while assimilated C surplus is stored in the roots. The transcriptomic analyses allowed us to identify root and leaf sets of genes whose expression depends on N availability. GO analyses of the identified genes revealed conserved biological functions involved in C and N metabolism and remobilization as well as other specifics such as the mitochondrial alternative respiration and chloroplastic cyclic electron flux. In addition, integrative analyses uncovered N regulated genes in root and leaf clusters, which are positively correlated with changes in the levels of different metabolites such as organic acids, amino acids, and formate. Interestingly, we identified transcription factors with high identity to TGA4, ARF8, HAT22, NF-YA5, and NLP9, which play key roles in N responses in Arabidopsis. Together, this study provides a set of nitrogen-responsive genes in tomato and new putative targets for tomato NUE and fruit quality improvement under limited N supply.

Highlights

Nitrogen (N) plays a crucial role in crop yield and quality [1,2]
We identified a group of tomato nitrogen transporter genes that might be involved in the remobilization and distribution of nitrogen compounds under limited N supply, and new regulatory factors such as SlTGA4, SlARF18, SlHAT22, SlNF-YA5, and SlNLP9, which might have a role in the control of longterm N response
Several reports have addressed the responses under N starvation conditions in different crops, but little is known about the integrative metabolic and transcriptomic adaptations under a limited nitrogen supply compatible with sustainable production

Summary

Introduction

Nitrogen (N) plays a crucial role in crop yield and quality [1,2]. Quantitatively, N is the most important mineral nutrient taken up by the plant and is a limiting factor in plant growth and development [3]. The use of nitrogen fertilizers worldwide exceeded 117 million tons in 2019 [5] and is projected to increase to 236 Mt by 2050 [6]. These inputs have led to environmental pollution, climate change, and, indirectly, biodiversity loss [7]. It has been estimated that less than half the N applied is taken up by crops [8], so there is margin for a drop in nitrogen inputs without compromising crop yields. The development of varieties with improved nitrogen use efficiency (NUE) would help to reduce fertilizer applications, lower energy costs, and greenhouse gas emissions and mitigate the consequences of nitrogen loss into soil and water sources [9]

Methods

Results

Conclusion