The Multiple Functions of the Nucleolus in Plant Development, Disease and Stress Responses

Abstract

The nucleolus is the most conspicuous domain in the eukaryotic cell nucleus, whose main function is ribosomal RNA (rRNA) synthesis and ribosome biogenesis. However, there is growing evidence that the nucleolus is also implicated in many other aspects of cell biology, such as regulation of cell cycle, growth and development, senescence, telomerase activity, gene silencing, responses to biotic and abiotic stresses. In the first part of the review, we briefly assess the traditional roles of the plant nucleolus in rRNA synthesis and ribosome biogenesis as well as possible functions in other RNA regulatory pathways such as splicing, nonsense-mediated mRNA decay and RNA silencing. In the second part of the review we summarize recent progress and discuss already known and new hypothetical roles of the nucleolus in plant growth and development. In addition, this part will highlight studies showing new nucleolar functions involved in responses to pathogen attack and abiotic stress. Cross-talk between the nucleolus and Cajal bodies is also discussed in the context of their association with poly(ADP ribose)polymerase (PARP), which is known to play a crucial role in various physiological processes including growth, development and responses to biotic and abiotic stresses.

Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors

“…These include nutrient starvation, changes in energy status, hypoxia, temperature changes, DNA damage, genotoxic stress, and other alterations to ribosome biogenesis factors. Disturbed ribosome biogenesis is typically accompanied by changes in nucleolar morphology and the activation of pathways leading to cell cycle arrest or apoptosis, which is commonly referred to as the ribosomal or nucleolar stress response (Boulon et al, 2010;Tsai and Pederson, 2014;Stepinski, 2016;Kalinina et al, 2018).…”

Interaction of a plant virus protein with the signature Cajal body protein coilin facilitates salicylic acid‐mediated plant defence responses

“…spliceosomal small nuclear RNPs, small nucleolar RNPs, telomerase and U7 snRNP) (for reviews see Gall, 2000;Carmo-Fonseca, 2002;Ogg & Lamond, 2002;Cioce & Lamond, 2005;Bassett, 2012). In addition to these well-recognized roles in RNA metabolism and RNA-protein assembly, a growing body of evidence indicates that the nucleolus and CBs also are involved in many other important cell functions such as cell cycle, growth, development and stress responses (Boulon et al, 2010;Bassett, 2012;Love et al, 2017;Kalinina et al, 2018). Thus, the nucleolus and CBs have emerged as multifunctional regulatory subnuclear domains, the roles of which in various biological processes we are just beginning to elucidate.…”

“…Several lines of evidence indicate that animal and plant virus proteins interact with the nucleolus to divert host nucleolar proteins from their natural functions in order to play novel role(s) in the virus infection cycle (Hiscox, 2007;Greco, 2009;Rajam€ aki & Valkonen, 2009;Taliansky et al, 2010;Wright et al, 2010;Semashko et al, 2012;Love et al, 2017;Kalinina et al, 2018). For example, the ability of the umbravirus groundnut rosette virus ORF3 protein to transport viral RNA long distances through the phloem, has been shown to depend strictly on its trafficking through the nucleolus and interaction with fibrillarin, the major nucleolar protein (Kim et al, 2007a,b;Canetta et al, 2008).…”

The Cajal Body in Plant-Virus Interactions

“…In plants, some elements of the RNA-directed DNA methylation (RdDM) pathway are concentrated in CBs [15,16], so this compartment has been proposed to be a site for the assembly of protein/RNA complexes mediating de novo DNA methylation [17,18]. In addition to the previously mentioned functions of CBs, these organelles also seem to influence cell cycle and DNA repair, growth, and developmental responses [2,11,19,20].…”