Apple vacuolar processing enzyme 4 is regulated by cysteine protease inhibitor and modulates fruit disease resistance

Abstract

Ring rot is a destructive apple disease caused by Botryosphaeria dothidea. The resistance mechanism of apple plants to B. dothidea remains unclear. Here, we show that apple vacuolar processing enzyme 4 (MdVPE4) is involved in fruit resistance to B. dothidea. MdVPE4 silencing reduced fruit resistance, whereas its overexpression improved fruit resistance. Gene expression analysis revealed that MdVPE4 influenced the expression of fruit resistance-related genes, such as apple polygalacturonase 1 (MdPG1), apple polygalacturonase inhibitor protein 1 (MdPGIP1), apple endochitinase 1 (MdCHI1), and apple thaumatin-like protein 1 (MdTHA1). The expression of the four genes responding to B. dothidea infection decreased in MdVPE4-silenced fruits. Further analysis demonstrated that B. dothidea infection induced MdVPE4 expression and enzyme activation in apple fruits. Moreover, MdVPE4 activity was modulated by apple cysteine proteinase inhibitor 1 (MdCPI1), which also contributed to fruit resistance to B. dothidea as revealed by gene overexpression and silencing analysis. MdCPI1 interacted with MdVPE4 and inhibited its activity. However, MdCPI1 expression was decreased by B. dothidea infection. Taken together, our findings indicate that the interaction of MdVPE4 and MdCPI1 plays an important role in modulating fruit resistance to B. dothidea.

Unraveling the Molecular Functions of Multifaced Plant‐Vacuolar Processing Enzymes

“…Furthermore, δvpe loss‐of‐function mutant in A. thaliana exhibited necrosis, curly leaf, and sensitive response to the aphid Myzus persicae infection (Alpuerto et al, 2017). Recently many reports have also shown the involvement of the VPEs in plant immunity against different pathogens, including Botryosphaeria dothiea (Dong et al, 2022), Phaeoisariopsis personata (Kumar et al, 2015), Phytophthora parasitica (Gao et al, 2023), Hyaloperonospora arabidopsidis (Misas‐Villamil et al, 2013), and Heterodera filipjevi (Labudda et al, 2020). In compliance with this observation, βVPE and γVPE expression increased mildly sets in A. thaliana treated with Heterodera schachtii , Verticillium dahile , and Colletotrichum tofieldiae in RNA seq‐data (Figure 5).…”

Vacuolar Processing Enzymes in Plant Programmed Cell Death and Autophagy

“…These ultrastructural analyses have shown the contribution of VPEs to vacuole collapse during PCD [ 35 ]. Further research has shown that VPEs are involved in plant defense against such pathogens as the bacterium Erwinia amylovora [ 62 ], nematode Heterodera filipjevi [ 63 ], the oomycetes Hyaloperonospora arabidopsidis [ 64 ] and Phytophthora parasitica [ 65 ], and the fungi Phaeoisariopsis personata [ 66 ], Fusarium oxysporum (FocTR4) [ 67 ] and Botryosphaeria dothidea [ 68 ].…”

Design, Synthesis, and Biological Evaluation of Novel Camphor-Based Hydrazide and Sulfonamide Derivatives as Laccase Inhibitors against Plant Pathogenic Fungi/Oomycetes

“…In the storage period or rainy year, the rate of rotten fruits often exceeds 80%, causing irreparable economic loss. 4 The serious consequences and high incidence have made the disease become a vital factor in restricting the development of the apple industry in China. 5 In addition, B. dothidea can infect some other commercial crops or fruits, including walnuts, pears, and blueberries.…”

“…Further, it also causes brown ring lesions and rot, making apple fruits inedible. In the storage period or rainy year, the rate of rotten fruits often exceeds 80%, causing irreparable economic loss . The serious consequences and high incidence have made the disease become a vital factor in restricting the development of the apple industry in China .…”