Abstract
BackgroundPlant nuclei superficially resemble animal and fungal nuclei, but the machinery and processes that underlie nuclear organization in these eukaryotic lineages appear to be evolutionarily distinct. Among the candidates for nuclear architectural elements in plants are coiled-coil proteins in the NMCP (Nuclear Matrix Constituent Protein) family. Using genetic and cytological approaches, we dissect the function of the four NMCP family proteins in Arabidopsis encoded by the CRWN genes, which were originally named LINC (LITTLE NUCLEI).ResultsCRWN proteins are essential for viability as evidenced by the inability to recover mutants that have disruptions in all four CRWN genes. Mutants deficient in different combinations of the four CRWN paralogs exhibit altered nuclear organization, including reduced nuclear size, aberrant nuclear shape and abnormal spatial organization of constitutive heterochromatin. Our results demonstrate functional diversification among CRWN paralogs; CRWN1 plays the predominant role in control of nuclear size and shape followed by CRWN4. Proper chromocenter organization is most sensitive to the deficiency of CRWN4. The reduction in nuclear volume in crwn mutants in the absence of a commensurate reduction in endoreduplication levels leads to an increase in average nuclear DNA density.ConclusionsOur findings indicate that CRWN proteins are important architectural components of plant nuclei that play diverse roles in both heterochromatin organization and the control of nuclear morphology.
Highlights
Plant nuclei superficially resemble animal and fungal nuclei, but the machinery and processes that underlie nuclear organization in these eukaryotic lineages appear to be evolutionarily distinct
Our findings demonstrate that CRWN proteins are essential for viability, and our analyses uncover complex functional diversification among CRWN proteins with regards to their effects on whole-plant morphology, nuclear size, and the spatial organization of constitutive heterochromatin aggregates in interphase nuclei
We found that CRWN1 plays the most prominent role among CRWN paralogs in controlling nuclear size, while CRWN4 has the most important role in controlling the distribution and number of heterochromatic chromocenters
Summary
Plant nuclei superficially resemble animal and fungal nuclei, but the machinery and processes that underlie nuclear organization in these eukaryotic lineages appear to be evolutionarily distinct. Despite similarities at the gross morphological level among all eukaryotic nuclei, such as a double-membrane boundary perforated with nuclear pores, most of the proteins known to affect nuclear structure in animals are not evolutionarily conserved and are difficult to recognize or absent entirely in plant proteomes [1,2,3] These observations indicate that the machinery, and perhaps the principles, specifying nuclear organization in flowering plants are distinct from those operating in animals and represent a convergent evolutionary path to a canonical nuclear organization in eukaryotic cells [4]. We demonstrated previously [5,6] that two paralogous Arabidopsis coiled-coil proteins, originally named LITTLE NUCLEI 1 and 2 (LINC1 & 2), play important roles in specifying nuclear shape and size Supporting this conclusion, Sakamoto and Takagi recently reported that disruption of LINC4, another of the four paralogous genes in this family, leads to reduced nuclear size and loss of elongated nuclear shape in differentiated cells, mirroring the phenotype of linc mutants [7]. More recent computational analysis [11], has suggested that the NMCP class of plant proteins shares more structural similarities to myosins or paramyosins than to lamins
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