Title: ANGUSTIFOLIA3 Signaling Coordinates Proliferation between Clonally Distinct Cells in Leaves
Abstract: Coordinated proliferation between clonally distinct cells via inter-cell-layer signaling largely determines the size and shape of plant organs [1Bai Y. Falk S. Schnittger A. Jakoby M.J. Hülskamp M. Tissue layer specific regulation of leaf length and width in Arabidopsis as revealed by the cell autonomous action of ANGUSTIFOLIA.Plant J. 2010; 61: 191-199Crossref PubMed Scopus (27) Google Scholar, 2Eriksson S. Stransfeld L. Adamski N.M. Breuninger H. Lenhard M. KLUH/CYP78A5-dependent growth signaling coordinates floral organ growth in Arabidopsis.Curr. Biol. 2010; 20: 527-532Abstract Full Text Full Text PDF PubMed Scopus (69) Google Scholar, 3Savaldi-Goldstein S. Chory J. Growth coordination and the shoot epidermis.Curr. Opin. Plant Biol. 2008; 11: 42-48Crossref PubMed Scopus (61) Google Scholar, 4Serralbo O. Pérez-Pérez J.M. Heidstra R. Scheres B. Non-cell-autonomous rescue of anaphase-promoting complex function revealed by mosaic analysis of HOBBIT, an Arabidopsis CDC27 homolog.Proc. Natl. Acad. Sci. USA. 2006; 103: 13250-13255Crossref PubMed Scopus (52) Google Scholar]. Nonetheless, the signaling mechanism underlying this coordination in leaves remains elusive because of a lack of understanding of the signaling molecule (or molecules) involved. ANGUSTIFOLIA3 (AN3, also called GRF-INTERACTING FACTOR1) encodes a putative transcriptional coactivator with homology to human synovial sarcoma translocation protein [5Kim J.H. Kende H. A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis.Proc. Natl. Acad. Sci. USA. 2004; 101: 13374-13379Crossref PubMed Scopus (288) Google Scholar, 6Horiguchi G. Kim G.T. Tsukaya H. The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana.Plant J. 2005; 43: 68-78Crossref PubMed Scopus (437) Google Scholar, 7Ichihashi Y. Kawade K. Usami T. Horiguchi G. Takahashi T. Tsukaya H. Key proliferative activity in the junction between the leaf blade and leaf petiole of Arabidopsis.Plant Physiol. 2011; 157: 1151-1162Crossref PubMed Scopus (71) Google Scholar]. AN3 transcripts accumulate in mesophyll cells but are not detectable in leaf epidermal cells [8Horiguchi G. Nakayama H. Ishikawa N. Kubo M. Demura T. Fukuda H. Tsukaya H. ANGUSTIFOLIA3 plays roles in adaxial/abaxial patterning and growth in leaf morphogenesis.Plant Cell Physiol. 2011; 52: 112-124Crossref PubMed Scopus (52) Google Scholar]. However, we found here that in addition to mesophyll cells [5Kim J.H. Kende H. A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis.Proc. Natl. Acad. Sci. USA. 2004; 101: 13374-13379Crossref PubMed Scopus (288) Google Scholar, 6Horiguchi G. Kim G.T. Tsukaya H. The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana.Plant J. 2005; 43: 68-78Crossref PubMed Scopus (437) Google Scholar], epidermal cells of an3 leaves show defective proliferation. This spatial difference between the accumulation pattern of AN3 transcripts and an3 leaf phenotype is explained by AN3 protein movement across cell layers. AN3 moves into epidermal cells after being synthesized within mesophyll cells and helps control epidermal cell proliferation. Interference with AN3 movement results in abnormal leaf size and shape, indicating that AN3 signaling is indispensable for normal leaf development. AN3 movement does not require type II chaperonin activity, which is needed for movement of some mobile proteins [9Xu X.M. Wang J. Xuan Z. Goldshmidt A. Borrill P.G. Hariharan N. Kim J.Y. Jackson D. Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function.Science. 2011; 333: 1141-1144Crossref PubMed Scopus (116) Google Scholar]. Taking these findings together, we present a novel model emphasizing the role of mesophyll cells as a signaling source coordinating proliferation between clonally independent leaf cells.