Dynamic Changes in Plant Nuclear Organization in Response to Environmental and Developmental Signals

Abstract

ORCID ID: 0000-0002-4141-5400 (I.M.).In both plants and animals, the nucleus acts as an organizing center for the changes that occur during an organism's life cycle, whether as part of a developmental program or in response to environmental factors. Here, we cover recent research that explores roles of the nucleus other than gene expression in light response, fertilization, plant-pathogen interactions, bacterial symbiotic events, and hormone signaling. New strides have been made in understanding subnuclear organization, how nuclear organization responds to different environments and developmental stages, and how the cytoplasm-nucleoplasm connections are made that allow these responses. We further highlight new tools that have been developed to study dynamic changes in nuclear organization.The nucleus is compartmentalized by a double membrane called the nuclear envelope (NE), which consists of the outer nuclear membrane (ONM), the inner nuclear membrane (INM), and the embedded nuclear pore complexes (NPCs). The NPC is the primary pathway of macromolecular transport between the nucleus and the cytoplasm and is conserved throughout eukaryotes. The ONM and INM are populated by a variety of membrane-associated proteins, and in particular the inner membrane hosts a specific subset of proteins (Starr and Fridolfsson, 2010;Meier et al., 2017). In addition to functioning in nuclear morphology, chromatin attachment, and likely signal transduction, plant NE-associated proteins are involved in nuclear positioning and movement within the larger cellular context (Griffis et al., 2014). While plant nuclear ultrastructure reveals an inner nuclear membrane-associated meshwork similar to the animal lamina, plant genomes do not encode obvious lamin homologs. Instead, plant-specific long coiled-coil proteins with structural similarity to animal lamins might contribute to this meshwork. Plants also lack centrosomes, and the NE plays a role as the microtubuleorganizing center at the onset of mitosis. NE proteins functioning as calcium channels are involved in perinuclear calcium oscillations, which are an important step in the establishment of plant-symbiont interactions (recently reviewed in Meier et al., 2017).While the nuclear periphery is emerging as an essential organizing platform for the nucleus, intranuclear functional and structural organization might also originate from independent self-assembly processes, with the most conspicuous manifestation of these processes revealed as the nucleolus. New methods are now robustly adapted for plants to reveal greater details of functional nuclear and nucleolar organization. Due to the increasing realization that spatial organization is a crucial part of biological function at the subcellular level, many of these aspects have been recently reviewed

Probing the 3D architecture of the plant nucleus with microscopy approaches: challenges and solutions

“…A major advance over recent decades has been a paradigm shift from a static to a dynamic view of nuclear organisation. Understanding the functional relationship between plasticity and dynamic processes, both at the nuclear and at the organismal level and during development and physiological adaptation, is a major challenge [3,7,26]. However, combined methodologies need to be applied and further developed to probe the plant cell nucleus in its full complexity during cellular responsesideally in a cell/tissuespecific manner.…”

MLKS2 is an ARM domain and F-actin-associated KASH protein that functions in stomatal complex development and meiotic chromosome segregation

“…The cytoplasmic N-terminal regions of KASH domain proteins interact directly or indirectly with a variety of cytoskeletal structures including motor proteins, microfilaments, microtubules, or intermediate filaments [5,16,27,28]. The forces generated by the cytoskeletal elements result in LINC-dependent movements known or thought to be required for specialized nuclear morphology associated with mitotic and meiotic cell division, karyogamy at fertilization, cell polarity, and response to biotic and abiotic interactions [27,[29][30][31][32].…”

The nuclear envelope in higher plant mitosis and meiosis

“…As mentioned above, SINE1 directly interacts with actin via its ARM domain. These nucleus-actin interactions are essential in anchoring and moving the nucleus in various developmental processes [32,33].…”