Polycomb repressive complex 2(PRC2)-mediated H3K27me3 deposition is vital for cell fate determination during Arabidopsis thaliana endosperm development.Unlike the transient endosperm in Arabidopsis,ce-reals follow a d...Polycomb repressive complex 2(PRC2)-mediated H3K27me3 deposition is vital for cell fate determination during Arabidopsis thaliana endosperm development.Unlike the transient endosperm in Arabidopsis,ce-reals follow a different developmental program after the cellularization phase,producing a persistent endo-sperm.In contrast to the single,constitutively expressed Fertilization Independent Endosperm(FIE)gene in Arabidopsis,cereals have evolved a duplicated,grain-specific counterpart,such as maize ZmFie1 and rice OsFie1.However,their functions remain unclear.We applied Cleavage Under Targets and Tagmentation(CUT&Tag)to profile the dynamics of the H3K27me3 mark during maize endosperm development.We observed a genome-wide elevation of H3K27me3 levels at early stages,followed by a rapid reduction after seed filling.We identified common regions and designated them as Filling Specific Peaks(FSPs),which are largely regulated by ZmFie1.Indeed,knockout of ZmFie1 results in earlier cellularization and slightly enhanced mitosis during endosperm filling,leading to smaller kernels that accumulate more zeins.Consis-tently,H3K27me3 levels onα-zein genes,located as tandem repeats on chromosome 4,are dramatically decreased in zmfie1.Moreover,it indirectly inhibits cell proliferation by mediating H3K27me3 deposition at ZmMADS loci,thereby balancing endosperm development and filling.Intriguingly,OsFie1 imposes H3K27me3 modification at the loci of 13-kDa prolamin genes and OsMADSs,leading to their repressed expression.Collectively,our findings reveal the conserved function of H3K27me3 deposition mediated by ZmFie1/OsFie1 in cereal endosperm development.The newly evolved,cereal grain-specific FIE1-PRC2 complex plays a key role in balancing storage substance synthesis and cell proliferation during persistent endosperm development.展开更多
基金sup-ported by the National Natural Science Foundation of China(U22A20466 to G.W.,32272146 and 31871626 to J.W.,32525007 to Y.W.)the Natural Science Foundation of Shanghai(23ZR1470400 to J.W.and 22ZR1469400 to Y.W.)+2 种基金the XPLORER PRIZE,NEW CORNERSTONE SCI-ENCE FOUNDATION(to Y.W.)the Shanghai Academy of Natural Sci-ences(SANS,to Y.W.)the Strategic Priority Research Program of the Chinese Academy of Sciences(XDB1120100 to Y.W.).
文摘Polycomb repressive complex 2(PRC2)-mediated H3K27me3 deposition is vital for cell fate determination during Arabidopsis thaliana endosperm development.Unlike the transient endosperm in Arabidopsis,ce-reals follow a different developmental program after the cellularization phase,producing a persistent endo-sperm.In contrast to the single,constitutively expressed Fertilization Independent Endosperm(FIE)gene in Arabidopsis,cereals have evolved a duplicated,grain-specific counterpart,such as maize ZmFie1 and rice OsFie1.However,their functions remain unclear.We applied Cleavage Under Targets and Tagmentation(CUT&Tag)to profile the dynamics of the H3K27me3 mark during maize endosperm development.We observed a genome-wide elevation of H3K27me3 levels at early stages,followed by a rapid reduction after seed filling.We identified common regions and designated them as Filling Specific Peaks(FSPs),which are largely regulated by ZmFie1.Indeed,knockout of ZmFie1 results in earlier cellularization and slightly enhanced mitosis during endosperm filling,leading to smaller kernels that accumulate more zeins.Consis-tently,H3K27me3 levels onα-zein genes,located as tandem repeats on chromosome 4,are dramatically decreased in zmfie1.Moreover,it indirectly inhibits cell proliferation by mediating H3K27me3 deposition at ZmMADS loci,thereby balancing endosperm development and filling.Intriguingly,OsFie1 imposes H3K27me3 modification at the loci of 13-kDa prolamin genes and OsMADSs,leading to their repressed expression.Collectively,our findings reveal the conserved function of H3K27me3 deposition mediated by ZmFie1/OsFie1 in cereal endosperm development.The newly evolved,cereal grain-specific FIE1-PRC2 complex plays a key role in balancing storage substance synthesis and cell proliferation during persistent endosperm development.