Loss of S-nitrosoglutathione reductase disturbs phytohormone homeostasis and regulates shoot side branching and fruit growth in tomato

Author(s):Show less -

Zuccarelli, Rafael ; Rodriguez-Ruiz, Marta ; Silva, Fernanda O. ; Gomes, Leticia D. L. ; Lopes-Oliveira, Patricia J. ; Zsogon, Agustin ; Andrade, Sonia C. S. ; Demarco, Diego ; Corpas, Francisco J. ; Peres, Lazaro E. P. ; Rossi, Magdalena ; Freschi, Luciano

• Document type: Journal article
• Source: Journal of Experimental Botany; v. N/A, p. 20-pg., 2023-05-09.

Abstract

S-Nitrosoglutathione plays a central role in nitric oxide (NO) homeostasis, and S-nitrosoglutathione reductase (GSNOR) regulates the cellular levels of S-nitrosoglutathione across kingdoms. Here, we investigated the role of endogenous NO in shaping shoot architecture and controlling fruit set and growth in tomato (Solanum lycopersicum). SlGSNOR silencing promoted shoot side branching and led to reduced fruit size, negatively impacting fruit yield. Greatly intensified in slgsnor knockout plants, these phenotypical changes were virtually unaffected by SlGSNOR overexpression. Silencing or knocking out of SlGSNOR intensified protein tyrosine nitration and S-nitrosation and led to aberrant auxin production and signaling in leaf primordia and fruit-setting ovaries, besides restricting the shoot basipetal polar auxin transport stream. SlGSNOR deficiency triggered extensive transcriptional reprogramming at early fruit development, reducing pericarp cell proliferation due to restrictions on auxin, gibberellin, and cytokinin production and signaling. Abnormal chloroplast development and carbon metabolism were also detected in early-developing NO-overaccumulating fruits, possibly limiting energy supply and building blocks for fruit growth. These findings provide new insights into the mechanisms by which endogenous NO fine-tunes the delicate hormonal network controlling shoot architecture, fruit set, and post-anthesis fruit development, emphasizing the relevance of NO-auxin interaction for plant development and productivity. Loss of S-nitrosoglutathione reductase, a key enzyme controlling nitric oxide homeostasis, promotes tomato shoot branching and restricts fruit development by disturbing auxin production and distribution. (AU)

• FAPESP's process: 18/16389-8 - Manipulation of light signaling and nitric oxide metabolism as a means of improving tomato quality traits
• Grantee: Luciano Freschi
• Support Opportunities: Regular Research Grants
• FAPESP's process: 20/03720-8 - Influence of nitric oxide (NO) manipulation in responses to different stresses in tomato
• Grantee: Patrícia Juliana Lopes Oliveira
• Support Opportunities: Scholarships in Brazil - Doctorate
• FAPESP's process: 21/05714-8 - Broadening the spectrum of nitric oxide action in plant photomorphogenesis and stress physiology
• Grantee: Luciano Freschi
• Support Opportunities: Regular Research Grants
• FAPESP's process: 16/01128-9 - Light and hormonal regulation of nutritional quality in Solanum lycopersicum
• Grantee: Maria Magdalena Rossi
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 18/06436-9 - Impacts of the manipulation of the GSNOR enzyme on a production, maturation pattern and resistance against phytopathogens in tomato fruits
• Grantee: Fernanda Oliveira da Silva
• Support Opportunities: Scholarships in Brazil - Scientific Initiation
• FAPESP's process: 16/02033-1 - Manipulation of nitric oxide levels and its impacts on tomato fruit physiology, hormonal balance and nutritional quality
• Grantee: Rafael Zuccarelli
• Support Opportunities: Scholarships in Brazil - Doctorate
• FAPESP's process: 17/17935-3 - SlGSNOR manipulation consequences on reactive oxygen and nitrogen species metabolism and on nitrated and nitrosylated proteins profiles along tomato fruit ripening
• Grantee: Marta Rodríguez Ruiz
• Support Opportunities: Scholarships in Brazil - Post-Doctoral