Cross-Talk Between Sporophyte and Gametophyte Generations Is Promoted by CHD3 Chromatin Remodelers inArabidopsis thaliana

Abstract

Angiosperm reproduction requires the integrated development of multiple tissues with different genotypes. To achieve successful fertilization, the haploid female gametophytes and diploid ovary must coordinate their development, after which the male gametes must navigate through the maternal sporophytic tissues to reach the female gametes. After fertilization, seed development requires coordinated development of the maternal diploid integuments, the triploid endosperm, and the diploid zygote. Transcription and signaling factors contribute to communication between these tissues, and roles for epigenetic regulation have been described for some of these processes. Here we identify a broad role for CHD3 chromatin remodelers in Arabidopsis thaliana reproductive development. Plants lacking the CHD3 remodeler, PICKLE, exhibit various reproductive defects including abnormal development of the integuments, female gametophyte, and pollen tube, as well as delayed progression of ovule and embryo development. Genetic analyses demonstrate that these phenotypes result from loss of PICKLE in the maternal sporophyte. The paralogous gene PICKLE RELATED 2 is preferentially expressed in the endosperm and acts antagonistically with respect to PICKLE in the seed: loss of PICKLE RELATED 2 suppresses the large seed phenotype of pickle seeds. Surprisingly, the alteration of seed size in pickle plants is sufficient to determine the expression of embryonic traits in the seedling primary root. These findings establish an important role for CHD3 remodelers in plant reproduction and highlight how the epigenetic status of one tissue can impact the development of genetically distinct tissues. KEYWORDS PICKLE; PKR2; ovule; pollen tube; seed size D EVELOPMENT in multicellular organisms requires coordinated morphogenesis and communication between tissues with distinct gene expression profiles and occasionally distinct genotypes. Mutations in epigenetic regulators can perturb mutually dependent cell types and therefore complicate interpretation of the resulting phenotypes. The reproductive system of flowering plants presents an attractive context in which to distinguish autonomous phenotypes from those arising from defects in ancillary tissues. The haploid male and female gametophyte generation is contained within the diploid sporophyte, and development of these genetically distinct tissues is highly interdependent (Ma and Sundaresan 2010;Niklas and Kutschera 2010). The female gametophyte develops within the sporophytic ovary, where it forms into an embryo sac as it is surrounded by the diploid sporophytic integuments of the ovule (Bencivenga et al. 2011;Chevalier et al. 2011). Characterization of ovule-defective mutants in Arabidopsis thaliana has revealed that female gametophyte development is dependent on the sporophyte, particularly integument development, and has also identified a variety of factors that contribute to this relationship including transcription factors, kinases, and components of plant hormone signal transduction pathwa...

Regulation of Plant Growth and Development: A Review From a Chromatin Remodeling Perspective

“…Studies of the CHD3 chromatin remodeler PICKLE ( PKL ) have highlighted its role in plant reproductive development by promoting crosstalk between the sporophytic and gametophytic generations. Loss of PKL in the maternal sporophyte leads to improper development of the Arabidopsis female gametophyte, integument and pollen tube, accompanied by delayed ovule and embryo development ( Carter et al, 2016 ).…”

Arabidopsis PIRL6 Is Essential for Male and Female Gametogenesis and Is Regulated by Alternative Splicing

“…Gametophyte development is dependent on the sporophyte and can be affected by sporophytic gene activity in premeiotic cells or in tissues neighboring the gametophytes (Olmedo-Monfil et al, 2010;Bencivenga et al, 2011;Forsthoefel and Vernon, 2011;Carter et al, 2016). However, both the expression and the segregation characteristics of PIRL6 fit the profile for a gametophyte gene.…”

Locus-specific paramutation in Zea mays is maintained by a PICKLE-like chromodomain helicase DNA-binding 3 protein controlling development and male gametophyte function

“…In addition to pkl mutants developing pickle-like root structures [ 63 ], they have reduced plant height [ 64 ], delayed vegetative phase change [ 65 ] and flowering [ 64 ], and reduced floral structures with aborted ovules [ 66 ]. These defects are similar to those displayed in rmr12 mutants ( Fig 1 ) consistent with pkl and rmr12 providing orthologous functions.…”