Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis.
Plant shoots are characterized by indeterminate growth resulting from the action of a population of stem cells in the shoot apical meristem (SAM). Indeterminacy within the SAM is specified in part by the class I knox homeobox genes. The myb domain proteins rough sheath2 (RS2) and ASYMMETRIC LEAVES1 (AS1) from maize (Zea mays) and Arabidopsis thaliana, respectively, are required to establish determinacy during leaf development. These proteins are part of a cellular memory system that in response to a stem cell-derived signal keeps knox genes in an off state during organogenesis. Here, we show that RS2/AS1 can form conserved protein complexes through interaction with the DNA binding factor ASYMMETRIC LEAVES2, a predicted RNA binding protein (RIK, for RS2-Interacting KH protein), and a homologue of the chromatin-remodeling protein HIRA. Partial loss of HIRA function in Arabidopsis results in developmental defects comparable to those of as1 and causes reactivation of knox genes in developing leaves, demonstrating a direct role for HIRA in knox gene repression and the establishment of determinacy during leaf formation. Our data suggest that RS2/AS1 and HIRA mediate the epigenetic silencing of knox genes, possibly by modulating chromatin structure. Components of this process are conserved in animals, suggesting the possibility that a similar epigenetic mechanism maintains determinacy during both plant and animal development.
Phelps-Durr
Tara L
TL
Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA.
Thomas
Julie
J
Vahab
Phil
P
Timmermans
Marja C P
MC
D017360:Arabidopsis / Q000196:embryology / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D018797:Cell Cycle Proteins / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D018506:Gene Expression Regulation, Plant / Q000502:physiology; D020868:Gene Silencing / Q000502:physiology*; D020570:Genes, myb / Q000235:genetics; D056488:Histone Chaperones; D006657:Histones / Q000378:metabolism; D018398:Homeodomain Proteins / Q000235:genetics / Q000378:metabolism*; D018519:Meristem / Q000196:embryology / Q000235:genetics / Q000378:metabolism; D018832:Molecular Chaperones / Q000235:genetics / Q000378:metabolism; D008969:Molecular Sequence Data; D010802:Phylogeny; D018515:Plant Leaves / Q000196:embryology / Q000235:genetics / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D018520:Plant Shoots / Q000196:embryology / Q000235:genetics / Q000378:metabolism; D012097:Repressor Proteins / Q000235:genetics / Q000378:metabolism*; D012639:Seeds / Q000235:genetics / Q000378:metabolism; D017386:Sequence Homology, Amino Acid; D013234:Stem Cells / Q000166:cytology / Q000378:metabolism; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*; D003313:Zea mays / Q000196:embryology / Q000235:genetics / Q000378:metabolism*
C456239:ASYMMETRIC LEAVES1 protein, Arabidopsis; D029681:Arabidopsis Proteins; D018797:Cell Cycle Proteins; C484187:Hira protein, mouse; D056488:Histone Chaperones; D006657:Histones; D018398:Homeodomain Proteins; C405985:Knox1 protein, plant; D018832:Molecular Chaperones; D010940:Plant Proteins; D012097:Repressor Proteins; D014157:Transcription Factors; C118404:rough sheath2 protein, Zea mays