Unlocking the role of novel primary/di-amine oxidases in crop improvement: tissue specificity leads to specific roles connected to abiotic stress, hormone responses and nitrogen sensing

Authors: UPADHYAY, RAKESH - Oak Ridge Institute For Science And Education (ORISE); Shao, Jonathan; Maul, Jude; Schomberg, Harry; Roberts, Daniel; Mattoo, Autar

Submitted to: Journal of Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/28/2024
Publication Date: 11/2/2024
Citation: Upadhyay, R.K., Shao, J.Y., Maul, J.E., Schomberg, H.H., Roberts, D.P., Mattoo, A.K. 2024. Unlocking the role of novel primary/di-amine oxidases in crop improvement: tissue specificity leads to specific roles connected to abiotic stress, hormone responses and nitrogen sensing. Journal of Plant Physiology. 303:154374. https://doi.org/10.1016/j.jplph.2024.154374.
DOI: https://doi.org/10.1016/j.jplph.2024.154374

Interpretive Summary: Abiotic stress and nutrient efficiency management is prime goal in the era of climate change for developing new germplasm. Scientist at USDA/ARS discovered a group of genes known as copper amine oxidases encoding genes in tomato, prominently expressed in root tissues. The root tissues are an important organ for acquiring water and nutrient for plants thereby affecting plant development and growth physiology and affects plant ability to respond to changing environments. This study shows that the expression of these genes is at higher levels during drought and heat stress responses and suppressed in response to external nitrogen availability. This multifactorial stress involvement of these genes makes them perfect target for genetics and plants breeding and biotechnological manipulations. This study will be helpful for scientist, farmers and plant breeder.

Technical Abstract: Genetic improvements of solanaceous crops for quality and stress response traits are needed because of the central role vegetables and fruits have in providing nutrients in human diets. Copper amine oxidase (CuAO) encoding genes involved in metabolism of primary/di-amine nitrogenous compounds play a role in balancing internal nitrogen (N) pools when external N supply fluctuates during growth, development and environmental stresses. In the present study, we investigated the occurrence, molecular evolution and possible role(s) of these unknown genes in tomato crops. Multiple genome-wide bioinformatics approaches led to the identification of eight bona fide CuAO genes (SlCuAO1–SlCuAO8) in the tomato genome with gene numbers like those in Arabidopsis and rice indicating their conserved functional relevance with a tandemly duplicated SlCuAO6-SlCuAO7 pair at chr.9. A conserved intron-exon size and phase distribution for SlCuAO2, 3, 4 pairs are like a recently identified single duckweed SpCuAO1 orthologue gene indicating its evolutionary conservation. Synteny analysis shows their closest association to Arabidopsis and not with rice. Transcriptome data indicates that gene expression for six genes (SlCuAO1, 2, 3, 4, 6, 7) is root specific, is fruit specific for SlCuAO5 and flower specific for SlCuAO8 thus indicating amine oxidation is variable across tissues with a prominance in root tissue. The majority of CuAO genes are negatively regulated by methyl jasmonate except a positive regulation for CuAO3/8. Transcript analysis from ethylene deficient transgenic lines indicates ethylene is required for activation of only SlCuAO4. Across various N regimes, CuAO4 and CuAO5 were the most significant tissue independent N responsive genes. Drought and heat stress identified CuAO5 as an overlapping highly expressed gene that collaborates with putrescine accumulation for free and conjugated forms with opposite abundance of bound forms. Taken together our study highlights new insights into roles of copper amine oxidation genes and identifies CuAO5 as a multiple stress-induced gene which can be used in genetic improvement programs for combining heat, drought and N use efficiency related traits.