Regulation of the seed to seedling developmental phase transition by the LAFL and VAL transcription factor networks

Focus Article

Donald R. McCarty, Masaharu Suzuki, Haiyan Jia

Published Online: Aug 23 2013

DOI: 10.1002/wdev.126

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In the seed, a fundamental transition between embryo and vegetative phases of plant development is coordinated by the interaction between the AFL and VAL sub‐clades of the plant specific B3 domain transcription factor family. The AFL B3 factors together with LEC1‐type HAP3 transcription factors promote embryo maturation; whereas the VAL B3 factors repress the LEC1/AFL (LAFL) network during seed germination. Recent advances reveal that genes in key developmental programs and hormone signaling pathways are downstream targets of the LAFL network highlighting the central role of the LAFL network in integration of intrinsic developmental and hormonal signals during plant development. The VAL B3 proteins are proposed to mediate repression by recruiting a histone deacetylase complex (HDAC) to LAFL genes that contain the Sph/RY cis‐element recognized by AFL and VAL B3‐DNA‐binding domains. In addition to VAL B3 factors, epigenetic mechanisms are implicated in maintaining repression of LAFL network during vegetative development. WIREs Dev Biol 2014, 3:135–145. doi: 10.1002/wdev.126 This article is categorized under: Plant Development > Fertilization, Embryogenesis, and Seed Development Plant Development > Vegetative Development

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Domain architectures of AFL and VAL B3 transcription factors. The AFL and VAL groups are sister clades in the ABI3/VP1 family of B3 proteins in Arabidopsis. AFL and VAL proteins have distinct domain architectures: B3 domain (dark), B1 (green), B2 (blue), A1 (purple), PHD‐L domain (red), CW domain (orange), and EAR motif (yellow). ABI3 has an N‐terminal co‐activator/co‐repressor (COAR) domain that physically interacts with ABI5‐related‐bZIP factors. VAL3 has an incomplete PHD‐L domain (dashed circle). AFL B3 domains specifically bind to the Sph/RY motif (CATGCA), and VAL B3 domains are proposed to bind the same motif. PHD and CW‐Zf domains are identified as the histone modification readers that recognize the H3K4me3 mark. VAL2 CW‐Zf interacts with HDA19 to repress target gene transcription (see text). EAR motif may mediate the interaction of VAL1 with co‐repressor SNL1 (see text).

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LAFL and VAL networks regulate the seed to seedling phase transition. Spatial and temporal patterns of LAFL gene expression are refined by mutual interactions. Important direct targets of LAFL factors include ( 1) SSP and LEA genes, (2) transcription factor genes that control seed specific processes including PEI1, CUC1, BBM, WRI1 and FLC, and (3) genes that function in major hormone metabolism and signaling pathways. AGL15, PHB/PHV, and MYB115/118 are proposed to act upstream of LAFL network. The LAFL network is repressed by VAL B3 factors and other repressors during seed germination to enable the transition to seedling development. VAL factors play a central role in repression of LAFL network in part by binding to the Sph/RY motif and recruiting an HDAC. The interaction of VAL B3 factors with HDAC may be mediated by the co‐repressor SNL1. PRC2 proteins (CLF/SWN/MEA/EMF2) add H3K27me3 marks to LAFL genes. Acting in concert with PRC2, PRC1 proteins (LHP1/ EMF1/RING1a‐b/BMI1a‐b) bind to H3K27me3 marks and deposit H2AK119ub1 to maintain a stable repressed state of LAFL genes. The CHD3 chromatin remodeling factors, PKL and PKR2, can indirectly promote H3K27me3 modification by up‐regulating genes encoding PRC2 proteins. PKL is also present in the promoter region of LEC1, LEC2 and FUS3 genes that are enriched for H3K27me3. RBR can interact with the promoter of ABI3, and is required for establishing H3K27me3 modification by cooperating with PRC2. The SNF2 chromatin remodeling ATPase, BRM, can repress seed maturation genes by physically interacting with their promoters. The plant‐specific trihelix factor, ASIL1, contributes to repression of LAFL genes by binding to the GT element (CGTGATT). miR166 indirectly represses LEC2 transcription by targeting upstream PHB and PHV. GA signaling enhances VAL and PKL repression of the LAFL network. Negative feedback loops: LAFL factors (FUS3 and LEC1) up‐regulate VAL1, RING1b, miR166, and PKL. Black lines with arrows indicate activation, and black lines ending with bars indicate repression. Inferred functions with less experimental evidence are indicated by dashed lines.

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