Organellar and Secretory Ribonucleases: Major Players in Plant RNA Homeostasis

During the last 20 years there has been an intense focus on posttranscriptional regulation of gene expression, and the role played by ribonucleases (RNases) in this process. Most research has centered on cytoplasmic and nuclear RNA decay enzymes, particularly those involved in mRNA regulation, and in proteins mediating nucleus-localized coding and noncoding RNA processing. These effortshave created a well-defined picture of RNA homeostasis in eukaryotes, including plants (Schmid and Jensen 2018; Sieburth and Vincent 2018; Towler and Newbury, 2018; Matsui et al., 2019). Thus, cytoplasmic degradation of mRNAs in plants (see Box 1), which involves deadenylation, decapping, and degradation by 3′-5′ and 5′-3′ exoribonucleases, has been extensively studied and reviewed (e.g. Zhang and Guo 2017; Sieburth and Vincent 2018; Sorenson et al., 2018; Lange et al., 2019). Similarly, different roles for the nuclear exosome and other RNases in nuclear RNA processing and decay have been established (Lange et al., 2014; Sikorska et al., 2017; Tomecki et al., 2017; Sáez-Vásquez and Delseny 2019). RNA decay mediated by small RNAs associated to RNA-induced silencing complexes and the processing and decay of small RNAs (sRNAs) have also been the focus of intense research efforts (Fukudome and Fukuhara 2017; Yu et al., 2017; Wang et al., 2019).On the other hand, RNases that do not reside in the cytoplasm or nucleus have received significant less attention, even though their activities are important for plant growth, development, and response to biotic and abiotic stimuli from the environment. As we will describe, organellar RNases are essential to maintain RNA homeostasis in chloroplasts and mitochondria. Plants also express members of the RNase T2 protein family, associated with the secretory pathway, which are involved in the maintenance of normal cellular homeostasis, with diverse roles, from stress responses to control of self-pollen rejection. This review will provide a summary of the present knowledge on these RNases, from enzymatic characterizations to biological functions, and highlight questions that should be addressed in the future.