Genome-Wide Identification and Functional Analysis of Polyamine Oxidase Genes in Maize Reveal Essential Roles in Abiotic Stress Tolerance

Abstract

Polyamines (PAs) play a critical role in growth and developmental processes and stress responses in plants. Polyamine oxidase (PAO) is a flavin adenine dinucleotide (FAD)-dependent enzyme that plays a major role in PA catabolism. Here, for the first time, PAO genes in maize were screened for the whole genome-wide and nine ZmPAO genes were identified in this study, named as ZmPAO1-9. Based on structural characteristics and a comparison of phylogenetic relationships of PAO gene families from seven representative species, all nine PAO proteins in maize were categorized into three distinct subfamilies. Further, chromosome location and schematic structure revealed an unevenly distribution on chromosomes and evolutionarily conserved structure features of ZmPAO genes in maize, respectively. Furthermore, transcriptome analysis demonstrated that ZmPAO genes showed differential expression patterns at diverse developmental stages of maize, suggesting that these genes may play functional developmental roles in multiple tissues. Further, through qRT-PCR validation, these genes were confirmed to be responsive to heat, drought and salinity stress treatments in three various tissues, indicating their potential roles in abiotic stress responses. Eventually, to verify the biological function of ZmPAO genes, the transgenic Arabidopsis plants overexpressing ZmPAO6 gene were constructed as a typical representative to explore functional roles in plants. The results demonstrated that overexpression of ZmPAO6 can confer enhanced heat tolerance through mediating polyamine catabolism in transgenic Arabidopsis, which might result in reduced H2O2 and MDA accumulation and alleviated chlorophyll degradation under heat stress treatment, indicating that ZmPAO6 may play a crucial role in enhancing heat tolerance of transgenic Arabidopsis through the involvement in various physiological processes. Further, the expression analysis of related genes of antioxidant enzymes including glutathione peroxidase (GPX) and ascorbate peroxidase (APX) demonstrated that ZmPAO6 can enhance heat resistance in transgenic Arabidopsis through modulating heat-induced H2O2 accumulation in polyamine catabolism. Taken together, our results are the first to report the ZmPAO6 gene response to heat stress in plants and will serve to present an important theoretical basis for further unraveling the function and regulatory mechanism of ZmPAO genes in growth, development and adaptation to abiotic stresses in maize.

Plant Peroxisomal Polyamine Oxidase: A Ubiquitous Enzyme Involved in Abiotic Stress Tolerance

“…The PAOs from Z. mays ( ZmPAO2 , ZmPAO3 , ZmPAO5 , ZmPAO8 , and ZmPAO9 ) are systemically expressed in all the vegetative tissues, while ZmPAO4 and ZmPAO6 are expressed specifically in roots and stems only. The expression of ZmPAO1 is restricted to seedlings only [ 54 , 57 ]. BdPAO1 and BdPAO2 from B. distachyon are found to be expressed in leaves, while BdPAO3 , BdPAO4 , and BdPAO5 are found to be expressed in inflorescence only [ 21 ].…”

Leaf Proteomic Analysis in Seedlings of Two Maize Landraces with Different Tolerance to Boron Toxicity

“…This enzyme catalyzes the back-conversion of spermine (Spm) to spermidine (Spd), and Spd to putrescine (Put) [ 49 ]. Maize polyamines play a crucial role in the abiotic stress response [ 33 ]. In fact, it has been reported that Put protects the plant’s photosynthetic apparatus against several abiotic stresses [ 50 ].…”

“…Maize is an important crop that provides approximately half of the calories consumed worldwide; in addition, it is one of the principal genetic model plants for crop improvement and food security [ 30 , 31 , 32 ]. However, maize production is seriously constrained by abiotic and biotic stresses [ 33 ]. In particular, B toxicity causes a decrease in maize production, as well as in other cereals [ 28 , 34 , 35 ].…”