Expression of AtCAN1 and AtCAN2 genes of the plant SNc nuclease family correlates with programmed cell death and endoreduplication, indicating their role in the recycling of nucleic acid components.

Abstract

BackgroundControlled degradation of genomic DNA is a common feature of all known cases of programmed cell death (PCD) in animals and plants. In plants, nucleic acid degradation during PCD facilitates the redistribution of their constituent building blocks. Previous studies have shown that nucleases from the S1/P1 family are involved in this process; however, due to the complexity of the process, it has been hypothesized that nucleases from other families, including staphylococcal-like nucleases (SNc), may also participate. In Arabidopsis, this family comprises two nucleases with atypical plasma membrane localization for this enzyme class: AtCAN1 and AtCAN2. ResultsUsing the promoter-driven GUS reporter assay, we showed that genes encoding SNc nucleases are expressed in tissues grouped into three main categories. The first category includes plant structures that are clear examples of organs undergoing PCD, such as the root cap, vascular bundle elements, the tapetum, maturing seed pods, and senescent leaves. The second category comprises cells whose function involves interaction with the external environment and which are susceptible to pathogen attack. This group includes root hairs, stomatal guard cells, and hydathodes. The third group of plant structures showing SNc nuclease activity consists of elements characterized by endoreduplication, i.e., stipules, trichomes, and the basal parts of the hypocotyl. The analysis of microarray and RNA-seq transcriptomic data further confirmed the expression of both SNc genes in these three categories. Moreover, we presented the effects of a mutation that eliminates AtCAN1 expression on plant development. ConclusionsOur studies show that SNc nucleases are as broadly involved in the DNA degradation during plant PCD as the previously reported S1/P1 proteins. The frequent overlap in their expression profiles suggests cooperative action. Whereas SNc nucleases localize to the plasma membrane, S1/P1 nucleases are nuclear, indicating distinct yet complementary nucleolytic pathways. We further demonstrate that SNc nucleases are specifically expressed in organs that do not undergo PCD but are characterized by endoreduplication, implicating them in an unexplored mechanism for redistributing polyploid DNA components.