Both maternally and paternally imprinted genes regulate seed development in rice

Abstract

Genetic imprinting refers to the unequal expression of paternal and maternal alleles of a gene in sexually reproducing organisms, including mammals and flowering plants. Although many imprinted genes have been identified in plants, the functions of these imprinted genes have remained largely uninvestigated. We report genome-wide analysis of gene expression, DNA methylation and small RNAs in the rice endosperm and functional tests of five imprinted genes during seed development using Clustered Regularly Interspaced Short Palindromic Repeats/CRISPR-associated gene9 (CRISPR/Cas9) gene editing technology. In the rice endosperm, we identified 162 maternally expressed genes (MEGs) and 95 paternally expressed genes (PEGs), which were associated with miniature inverted-repeat transposable elements, imprinted differentially methylated loci and some 21-22 small interfering RNAs (siRNAs) and long noncoding RNAs (lncRNAs). Remarkably, one-third of MEGs and nearly one-half of PEGs were associated with grain yield quantitative trait loci. Most MEGs and some PEGs were expressed specifically in the endosperm. Disruption of two MEGs increased the amount of small starch granules and reduced grain and embryo size, whereas mutation of three PEGs reduced starch content and seed fertility. Our data indicate that both MEGs and PEGs in rice regulate nutrient metabolism and endosperm development, which optimize seed development and offspring fitness to facilitate parental-offspring coadaptation. These imprinted genes and mechanisms could be used to improve the grain yield of rice and other cereal crops.

Asymmetrical changes of gene expression, small RNAs and chromatin in two resynthesized wheat allotetraploids

“…In wheat allotetraploids, the dramatic changes in small RNAs and chromatin modifications such as H3K9me2 in AADD could alter the expression of TEs and the formation of aneuploids in AADD (Zhang et al, 2013), which is also a factor behind genome instability. Activation of TE is commonly observed during seed development in Arabidopsis (Gehring et al, 2009;Hsieh et al, 2009), soybean (Lin et al, 2017) and rice (Luo et al, 2011;Yuan et al, 2017). Activation of TEs in vegetative tissues is rare; however, a recent study found that activation of TEs in rice roots could act as a decoy for microRNA regulation (Cho and Paszkowski, 2017).…”

Wild tomato endosperm transcriptomes reveal common roles of genomic imprinting in both nuclear and cellular endosperm

“…We created an inventory of published IGs identified in A. thaliana ( At ; Köhler et al ., ; Spillane et al ., ; Gehring et al ., ; Hsieh et al ., ; McKeown et al ., ; Wolff et al ., ; Bratzel et al ., ; Pignatta et al ., ; Burkart‐Waco et al ., ; Jeong et al ., ), A. lyrata ( Al ; Klosinska et al ., ), C. rubella ( Cr ; Hatorangan et al ., ), rice ( Os ; Luo et al ., ; Yuan et al ., ), maize ( Zm ; Gutiérrez‐Marcos et al ., ; Zhang et al ., , ; Waters et al ., ; Xin et al ., ), S. bicolor ( Sb ; Zhang et al ., ) and castor bean ( Rc ; Xu et al ., ). Sequences were retrieved from public databases: At , The Arabidopsis Information Resource (TAIR; Swarbreck et al ., ) at http://www.arabidopsis.org; Al and Cr , Phytozome v11.0 (Goodstein et al ., ) at https://phytozome.jgi.doe.gov; maize, MaizeGDB (Lawrence, ) at http://www.maizegdb.org; rice and Sb , PlantGDB (Duvick et al ., ) at http://www.plantgdb.org; and Rc , Castor Bean Genome Project (Chan et al ., ) at http://castorbean.jcvi.org.…”

“…The kin conflict theory further predicts that imprinting will evolve under strong selective constraints in outcrossing lineages with high levels of multiple paternity, while such constraints might be relaxed under long‐term inbreeding (Brandvain and Haig, ). To our knowledge, genomic imprinting in the endosperm has been studied in representatives of four angiosperm families (Brassicaceae, Poaceae, Solanaceae and Euphorbiaceae), including: (i) (mainly) inbreeding species such as A. thaliana (Wolff et al ., ; Pignatta et al ., ), Capsella rubella (Hatorangan et al ., ) and rice (Yuan et al ., ); and (ii) (mainly) outcrossing species such as Arabidopsis lyrata (Klosinska et al ., ), maize (Zhang et al ., ), Sorghum bicolor (Zhang et al ., ), Solanum peruvianum (Florez‐Rueda et al ., ) and castor bean (Xu et al ., ). While seed phenotypes of homoploid crosses between closely‐related species with different mating systems are consistent with predictions of the kin conflict theory, they have hitherto not been associated with specific imprinting patterns (Rebernig et al ., ; Lafon‐Placette et al ., ).…”

Characterization of imprinted genes in rice reveals post-fertilization regulation and conservation at some loci of imprinting in plant species

“…Approximately 74% (53/72) PEGs and 53% (49/93) MEGs they identified were overlapped with the ones identified in the present study (Figure 1F). Similarly, about 80% (76/97) PEGs and 44% (72/162) MEGs discovered from L0-0L (Yuan et al, 2017) were included in our candidates list (Figure 1F), nevertheless, overlaps between N9-9N and L0-0L were much less (Yuan et al, 2017). The results indicated that we discovered more candidates than previous studies, and many of the imprinted genes identified before were included in our candidates list.…”

“…In light of the observations that indica/indica crosses (WW and RR) exhibited faster early endosperm development than the japonica/japonica crosses (LL and YY), and the hybrid seeds were more like their maternal parent (Figure 1A and B), we assumed that the deviation of maternal contribution at 5 DAF could be caused by slower endosperm development when japonica rice was used as the mother, which led to a slower maternal-to-zygotic transition. To confirm this hypothesis, we reanalyzed the RNA-seq data of the 7 DAF endosperm from the Longtepu ( indica ) and 02428 ( japonica ) reciprocal crosses (L0-0L)(Yuan et al, 2017). Consistent to our hypothesis, when the japonica rice 02428 used as the mother, the distribution peak of (maternal transcripts): (maternal transcripts + paternal transcripts) shifted to 0.75 (Figure 1E).…”