0
Views
0
CrossRef citations to date
0
Altmetric
Short Communication

CLE peptides act via the receptor-like kinase CRINKLY 4 in Physcomitrium patens gametophore development

ORCID Icon, ORCID Icon & ORCID Icon
Article: 2386502 | Received 30 May 2024, Accepted 25 Jul 2024, Published online: 31 Jul 2024

References

  • Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science. 1999;283(5409):1911–8. doi:10.1126/science.283.5409.1911.
  • Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu C-M. The 14–amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell. 2005;17(9):2542–2553. doi:10.1105/tpc.105.034009.
  • Hobe M, Müller R, Grünewald M, Brand U, Simon R. Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol. 2003;213(8):371–381. doi:10.1007/s00427-003-0329-5.
  • Stahl Y, Wink RH, Ingram G, Simon R. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol. 2009;19(11):909–914. doi:10.1016/j.cub.2009.03.060.
  • Narasimhan M, Simon R. Spatial range, temporal span, and promiscuity of CLE-RLK signaling. Front Plant Sci. 2022;13:13. doi:10.3389/fpls.2022.906087.
  • Demesa-Arevalo E, Narasimhan M, Simon R. Intercellular communication in shoot meristems. Annu Rev Plant Biol. 2024;75(1):319–344. doi:10.1146/annurev-arplant-070523.
  • Cock JM, Mccormick S. A large family of genes that share homology with CLAVATA3. Plant Physiol. 2001;126(3):939–942. doi:10.1104/pp.126.3.939.
  • Fletcher JC. Recent advances in Arabidopsis CLE peptide signaling. Trends Plant Sci. 2020;25(10):1005–1016. doi:10.1016/j.tplants.2020.04.014.
  • Trotochaud AE, Hao T, Wu G, Yang Z, Clark SE. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a rho-related protein. Plant Cell. 1999;11(3):393–405. doi:10.1105/tpc.11.3.393.
  • Müller R, Bleckmann A, Simon R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell. 2008;20(4):934–946. doi:10.1105/tpc.107.057547.
  • DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J. 2006;45(1):1–16. doi:10.1111/j.1365-313X.2005.02592.x.
  • Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, Simon R, Yamaguchi-Shinozaki K, Fukuda H, Sawa S, et al. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development. 2010;137(22):3911–3920. doi:10.1242/dev.061747.
  • Shimizu N, Ishida T, Yamada M, Shigenobu S, Tabata R, Kinoshita A, Yamaguchi K, Hasebe M, Mitsumasu K, Sawa S, et al. BAM 1 and receptor-like protein kinase 2 constitute a signaling pathway and modulate CLE peptide-triggered growth inhibition in Arabidopsis root. New Phytol. 2015;208(4):1104–1113. doi:10.1111/nph.13520.
  • Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science. 2000;289(5479):617–619. doi:10.1126/science.289.5479.617.
  • Schoof H, Lenhard M, Haecker A, Mayer KFX, Jürgens G, Laux T. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell. 2000;100(6):635–644. doi:10.1016/S0092-8674(00)80700-X.
  • Somssich M, Il JB, Simon R, Jackson D. CLAVATA-WUSCHEL signaling in the shoot meristem. Development. 2016;143(18):3238–3248. doi:10.1242/dev.133645.
  • Stahl Y, Grabowski S, Bleckmann A, Kühnemuth R, Weidtkamp-Peters S, Pinto K, Kirschner G, Schmid J, Wink R, Hülsewede A, et al. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol. 2013;23(5):362–371. doi:10.1016/j.cub.2013.01.045.
  • Becraft P, Stinard P, McCarty D. CRINKLY4: a TNFR-Like receptor kinase involved in maize epidermal differentiation. Science. 1996;273(5280):1406–1409. doi:10.1126/science.273.5280.1406.
  • Becraft PW, Asuncion-Crabb Y. Positional cues specify and maintain aleurone cell fate in maize endosperm development. Development. 2000;127(18):4039–4048. doi:10.1242/dev.127.18.4039.
  • Gifford ML, Dean S, Ingram G. The Arabidopsis ACR4 gene plays a role in cell layer organisation during ovule integument and sepal margin development. Development. 2003;130(8):4249–4258. doi:10.1242/dev.00634.
  • Ingram G. Epidermal signalling and the control of plant shoot growth. Plant Cell Monogr. 2007;10127–10153. doi:10.1007/7089_2007_140.
  • Watanabe M, Tanaka H, Watanabe D, Machida C, Machida Y. The ACR4 receptor-like kinase is required for surface formation of epidermis-related tissues in Arabidopsis thaliana. Plant J. 2004;39(3):298–308. doi:10.1111/j.1365-313X.2004.02132.x.
  • Roeder AHK, Cunha A, Ohno CK, Meyerowitz EM. Cell cycle regulates cell type in the Arabidopsis sepal. Development. 2012;139(23):4416–4427. doi:10.1242/dev.082925.
  • Cao X, Li K, Suh SG, Guo T, Becraft PW. Molecular analysis of the CRINKLY4 gene family in Arabidopsis thaliana. Planta. 2005;220(5):645–657. doi:10.1007/s00425-004-1378-3.
  • Tanaka H, Watanabe M, Watanabe D, Tanaka T, Machida C, Machida Y. ACR4, a putative receptor kinase gene of Arabidopsis thaliana, that is expressed in the outer cell layers of embryos and plants, is involved in proper embryogenesis. Plant Cell Physiol. 2002;43(4):419–428. doi:10.1093/PCP/PCF052.
  • Tian Q, Olsen L, Sun B, Lid SE, Brown RC, Lemmon BE, Fosnes K, Gruis D, Opsahl-Sorteberg H-G, Otegui MS, et al. Subcellular localization and functional domain studies of DEFECTIVE KERNEL1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. Plant Cell. 2007;19(10):3127–3145. doi:10.1105/tpc.106.048868.
  • De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, et al. Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science. 2008;322(5901):594–597. doi:10.1126/science.1160158.
  • Johnson KL, Degnan KA, Ross Walker J, Ingram GC. AtDEK1 is essential for specification of embryonic epidermal cell fate. Plant J. 2005;44(1):114–127. doi:10.1111/j.1365-313x.2005.02514.x.
  • Galletti R, Johnson KL, Scofield S, San-Bento R, Watt AM, Murray JAH, Ingram GC. DEFECTIVE KERNEL 1 promotes and maintains plant epidermal differentiation. Development. 2015;142(11):1978–1983. doi:10.1242/dev.122325.
  • Perroud P, Demko V, Johansen W, Wilson RC, Olsen O-A, Quatrano RS. Defective Kernel 1 (DEK1) is required for three-dimensional growth in Physcomitrella patens. New Phytol. 2014;203(3):794–804. doi:10.1111/nph.12844.
  • Kofuji R, Hasebe M. Eight types of stem cells in the life cycle of the moss Physcomitrella patens. Curr Opin Plant Biol. 2014;17:13–21. doi:10.1016/j.pbi.2013.10.007.
  • Moody LA. The 2D to 3D growth transition in the moss Physcomitrella patens. Curr Opin Plant Biol. 2019;47:88–95. doi:10.1016/j.pbi.2018.10.001.
  • Moody LA, Kelly S, Rabbinowitsch EH, Langdale JA. Genetic regulation of the 2D to 3D growth transition in the moss Physcomitrella patens. Curr Biol. 2018;28(3):473–478.e5. doi:10.1016/j.cub.2017.12.052.
  • Aoyama T, Hiwatashi Y, Shigyo M, Kofuji R, Kubo M, Ito M, Hasebe M. AP2-type transcription factors determine stem cell identity in the moss Physcomitrella patens. Development. 2012;139(17):3120–3129. doi:10.1242/dev.076091.
  • Harrison C, Roeder AH, Meyerowitz E, Langdale JA. Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Curr Biol. 2009;19(6):461–471. doi:10.1016/j.cub.2009.02.050.
  • Ishikawa M, Fujiwara A, Kosetsu K, Horiuchi Y, Kamamoto N, Umakawa N, Tamada Y, Zhang L, Matsushita K, Palfalvi G, et al. GRAS transcription factors regulate cell division planes in moss overriding the default rule. Proc Natl Acad Sci USA. 2023;120(4). doi:10.1073/pnas.2210632120.
  • Xu B, Ohtani M, Yamaguchi M, Toyooka K, Wakazaki M, Sato M, Kubo M, Nakano Y, Sano R, Hiwatashi Y, et al. Contribution of NAC transcription factors to plant adaptation to land. Science. 2014;343(6178):1505–1508. doi:10.1126/science.1248417.
  • Rensing SA, Goffinet B, Meyberg R, Wu S-Z, Bezanilla M. The moss Physcomitrium (Physcomitrella) patens: a model organism for non-seed plants. Plant Cell. 2020;32(5):1361–1376. doi:10.1105/tpc.19.00828.
  • Cove DJ, Perroud PF, Charron J, McDaniel SF, Khandelwal A, Quatrano RS. The moss Physcomitrella patens: a novel model system for plant development and genomic studies. Cold Spring Harb Protoc. 2009;2009(2):pdb.emo115. doi:10.1101/pdb.emo115.
  • Whitewoods CD, Cammarata J, Nemec Venza Z, Sang S, Crook AD, Aoyama T, Wang XY, Waller M, Kamisugi Y, Cuming AC, et al. CLAVATA was a genetic novelty for the morphological innovation of 3D growth in land plants. Curr Biol. 2018;28(15):2365–2376.e5. doi:10.1016/j.cub.2018.05.068.
  • Nemec-Venza Z, Madden C, Stewart A, Liu W, Novák O, Pěnčík A, Cuming AC, Kamisugi Y, Harrison CJ. CLAVATA modulates auxin homeostasis and transport to regulate stem cell identity and plant shape in a moss. New Phytol. 2022;234(1):149–163. doi:10.1111/nph.17969.
  • Cammarata J, Morales Farfan C, Scanlon MJ, Roeder AHK. Cytokinin–CLAVATA cross-talk is an ancient mechanism regulating shoot meristem homeostasis in land plants. Proc Natl Acad Sci USA. 2022;119(14). doi:10.1073/pnas.2116860119.
  • Nemec Venza Z, Greiff GRL, Harrison J. Mutant phenotypes and comprehensive expression analyses reveal roles for CLAVATA in moss vegetative 2 and reproductive development and fertility. bioRxiv. 2024; doi:10.1101/2024.04.05.585946.
  • Demko V, Belova T, Messerer M, Hvidsten TR, Perroud P-F, Ako AE, Johansen W, Mayer KFX, Olsen O-A, Lang D, et al. Regulation of developmental gatekeeping and cell fate transition by the calpain protease DEK1 in Physcomitrium patens. Commun Biol. 2024;7(1). doi:10.1038/s42003-024-05933-z.
  • Demko V, Ako E, Perroud PF, Quatrano R, Olsen O-A. The phenotype of the CRINKLY4 deletion mutant of Physcomitrella patens suggests a broad role in developmental regulation in early land plants. Planta. 2016;244(1):275–284. doi:10.1007/s00425-016-2526-2.
  • Ashton N, Cove D. The isolation and preliminary characterisation of auxotrophic and analogue resistant mutants of the moss, Physcomitrella patens. Mol Gen Genet. 2004;154(1):87–95. doi:10.1007/BF00265581.
  • Johansen W, Ako AE, Demko V, Perroud P-F, Rensing SA, Mekhlif AK, Olsen O-A. The DEK1 calpain linker functions in three-dimensional body patterning in Physcomitrella patens. Plant Physiol. 2016;172(2):1089–1104. doi:10.1104/pp.16.00925.
  • Olsen OA, Perroud PF, Johansen W, Demko V. DEK1; missing piece in puzzle of plant development. Trends Plant Sci. 2015;20(2):70–71. doi:10.1016/j.tplants.2015.01.003.
  • Barker EI, Ashton NW. Heteroblasty in the moss, Aphanoregma patens (Physcomitrella patens), results from progressive modulation of a single fundamental leaf developmental programme. J Bryol. 2013;35(3):185–196. doi:10.1179/1743282013Y.0000000058.
  • Dennis RJ, Whitewoods CD, Harrison CJ. Quantitative methods in like-for-like comparative analyses of Aphanorrhegma (Physcomitrella) patens phyllid development. J Bryol. 2019;41(4):314–321. doi:10.1080/03736687.2019.1668109.
  • Lin W, Wang Y, Coudert Y, Kierzkowski D. Leaf morphogenesis: insights from the moss Physcomitrium patens. Front Plant Sci. 2021;12:12. doi:10.3389/fpls.2021.736212.
  • Nodine MD, Tax FE. Two receptor-like kinases required together for the establishment of Arabidopsis cotyledon primordia. Dev Biol. 2008;314(1):161–170. doi:10.1016/j.ydbio.2007.11.021.
  • San-Bento R, Farcot E, Galletti R, Creff A, Ingram G. Epidermal identity is maintained by cell–cell communication via a universally active feedback loop in Arabidopsis thaliana. Plant J. 2014;77(1):46–58. doi:10.1111/tpj.12360.