ACAULIS5 Is Required for Cytokinin Accumulation and Function During Secondary Growth of Populus Trees

. 2020 ; 11 () : 601858. [epub] 20201116

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33304375

In the primary root and young hypocotyl of Arabidopsis, ACAULIS5 promotes translation of SUPPRESSOR OF ACAULIS51 (SAC51) and thereby inhibits cytokinin biosynthesis and vascular cell division. In this study, the relationships between ACAULIS5, SAC51 and cytokinin biosynthesis were investigated during secondary growth of Populus stems. Overexpression of ACAULIS5 from the constitutive 35S promoter in hybrid aspen (Populus tremula × Populus tremuloides) trees suppressed the expression level of ACAULIS5, which resulted in low levels of the physiologically active cytokinin bases as well as their direct riboside precursors in the transgenic lines. Low ACAULIS5 expression and low cytokinin levels of the transgenic trees coincided with low cambial activity of the stem. ACAULIS5 therefore, contrary to its function in young seedlings in Arabidopsis, stimulates cytokinin accumulation and cambial activity during secondary growth of the stem. This function is not derived from maturing secondary xylem tissues as transgenic suppression of ACAULIS5 levels in these tissues did not influence secondary growth. Interestingly, evidence was obtained for increased activity of the anticlinal division of the cambial initials under conditions of low ACAULIS5 expression and low cytokinin accumulation. We propose that ACAULIS5 integrates auxin and cytokinin signaling to promote extensive secondary growth of tree stems.

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Agustí J., Herold S., Schwarz M., Sanchez P., Ljung K., Dun E. A., et al. (2011). Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. PNAS 108 20242–20247. 10.1073/pnas.1111902108 PubMed DOI PMC

Antoniadi I., Plaèková L., Simonovik B., Doležal K., Turnbull C., Ljung K., et al. (2015). Cell-type-specific cytokinin distribution within the Arabidopsis primary root apex. Plant Cell 27 1955–1967. 10.1105/tpc.15.00176 PubMed DOI PMC

Baima S., Forte V., Possenti M., Peñalosa A., Leoni G., Salvi S., et al. (2014). Negative feedback regulation of auxin signaling by ATHB8/ACL5-BUD2 transcription module. Mol. Plant 7 1006–1025. 10.1093/mp/ssu051 PubMed DOI

Bollhöner B., Jokipii-Lukkari S., Bygdell J., Stael S., Adriasola M., Muñiz L., et al. (2018). The function of two type II metacaspases in woody tissues of Populus trees. New Phytol. 217 1551–1565. 10.1111/nph.14945 PubMed DOI

Chang S. J., Puryear J., Cairney J. (1993). A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11 113–116. 10.1007/bf02670468 DOI

Clay N. K., Nelson T. (2005). Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. Plant Physiol. 138 767–777. 10.1104/pp.104.055756 PubMed DOI PMC

de Rybel B., Adibi M., Breda A. S., Wendrich J. R., Smit M. E., Novák O., et al. (2014). Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science 345:1255215. 10.1126/science.1255215 PubMed DOI

Endo S., Iwamoto K., Fukuda H. (2018). Overexpression and cosuppression of xylem-related genes in an early xylem differentiation stage-specific manner by the AtTED4 promoter. Plant Biotechnol. J. 16 451–458. 10.1111/pbi.12784 PubMed DOI PMC

Etchells J. P., Provost C. M., Turner S. R. (2012). Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling. PLoS Genet. 8:e1002997. 10.1371/journal.pgen.1002997 PubMed DOI PMC

Fischer U., Kucukoglu M., Helariutta Y., Bhalerao R. P. (2019). The dynamics of cambial stem cell activity. Annu. Rev. Plant Biol. 70 293–319. 10.1146/annurev-arplant-050718-100402 PubMed DOI

Hanzawa Y., Takahashi T., Komeda Y. (1997). ACL5: an Arabidopsis gene required for internodal elongation after flowering. Plant J. 12 863–874. 10.1046/j.1365-313x.1997.12040863.x PubMed DOI

Hanzawa Y., Takahashi T., Michael A. J., Burtin D., Long D., Pineiro M., et al. (2000). ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J. 19 4248–4256. 10.1093/emboj/19.16.4248 PubMed DOI PMC

Imai A., Hanzawa Y., Komura M., Yamamoto K. T., Komeda Y., Takahashi T. (2006). The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133 3575–3585. 10.1242/dev.02535 PubMed DOI

Imai A., Komura M., Kawano E., Kuwashiro Y., Takahashi T. (2008). A semi-dominant mutation in the ribosomal protein L10 gene suppresses the dwarf phenotype of the acl5 mutant in Arabidopsis thaliana. Plant J. 56 881–890. 10.1111/j.1365-313x.2008.03647.x PubMed DOI

Immanen J., Nieminen K., Duchens Silva H., Rodríguez Rojas F., Meisel L. A., Silva H., et al. (2013). Characterization of cytokinin signaling and homeostasis gene families in two hardwood tree species: Populus trichocarpa and Prunus persica. BMC Genomics 14:885. 10.1186/1471-2164-14-885 PubMed DOI PMC

Immanen J., Nieminen K., Smolander O. P., Kojima M., Alonso Serra J., Koskinen P., et al. (2016). Cytokinin and auxin display distinct but interconnected distribution and signaling profiles to stimulate cambial activity. Curr. Biol. 26 1990–1997. 10.1016/j.cub.2016.05.053 PubMed DOI

Kakehi J., Kawano E., Yoshimoto K., Cai Q., Imai A., Takahashi T. (2015). Mutations in ribosomal proteins, RPL4 and RACK1, suppress the phenotype of a thermospermine-deficient mutant of Arabidopsis thaliana. PLoS One 10:e0117309. 10.1371/journal.pone.0117309 PubMed DOI PMC

Karimi M., Inzé D., Depicker A. (2002). GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7 193–195. 10.1016/s1360-1385(02)02251-3 PubMed DOI

Knott J. M., Romer P., Sumper M. (2007). Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett. 581 3081–3086. 10.1016/j.febslet.2007.05.074 PubMed DOI

Koncz C., Schell J. (1986). The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204 383–396. 10.1007/bf00331014 DOI

Larson P. R. (1994). The Vascular Cambium: Development and Structure. Berlin: Springer.

Livak K. J., Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔCT) Method. Methods 25 402–408. 10.1006/meth.2001.1262 PubMed DOI

Milhinhos A., Prestele J., Bollhöner B., Matos A., Vera-Sirera F., Ljung K., et al. (2013). Thermospermine levels are controlled by an auxin-dependent feedback-loop mechanism in Populus xylem. Plant J. 75 685–698. 10.1111/tpj.12231 PubMed DOI

Milhinhos A., Vera-Sirera F., Blanco-Tourinan N., Mari-Carmona C., Carrio-Segui A., Forment J., et al. (2019). SOBIR1/EVR prevents precocious initiation of fiber differentiation during wood development through a mechanism involving BP and ERECTA. Proc. Natl. Acad. Sci. U.S.A. 116, 18710– 18716. 10.1073/pnas.1807863116 PubMed DOI PMC

Muñiz L., Minguet E. G., Singh Kumar S., Pesquet E., Vera-Sirera F., Courtois-Moreau C., et al. (2008). ACAULIS 5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135 2573–2582. 10.1242/dev.019349 PubMed DOI

Murashige T., Skoog F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15 473–497. 10.1111/j.1399-3054.1962.tb08052.x DOI

Nieminen K., Immanen J., Laxell M., Kauppinen L., Tarkowski P., Dolezal K., et al. (2008). Cytokinin signaling regulates cambial development in poplar. Proc. Natl. Acad. Sci. U.S.A. 105 20032–20037. 10.1073/pnas.0805617106 PubMed DOI PMC

Nilsson O., Aldén T., Sitbon F., Little C. H. A., Chalupa V., Sandberg G., et al. (1992). Spatial pattern of cauliflower mosaic virus 35S promoter–luciferase expression in transgenic hybrid aspen trees monitored by enzymatic assay and non-destructive imaging. Transgen. Res. 1 209–220. 10.1007/bf02524751 DOI

Ohashi-Ito K., Saegusa M., Iwamoto K., Oda Y., Katayama H., Kojima M., et al. (2014). A bHLH complex activates vascular cell division via cytokinin action in root apical meristem. Curr. Biol. 24 2053–2058. 10.1016/j.cub.2014.07.050 PubMed DOI

Ragni L., Nieminen K., Pacheco-Villalobos D., Sibout R., Schwechheimer C., Hardtke C. S. (2011). Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion. Plant Cell 23 1322–1336. 10.1105/tpc.111.084020 PubMed DOI PMC

Ramírez-Carvajal G. A., Morse A. M., Davis J. M. (2008). Transcript profiles of the cytokinin response regulator gene family in Populus imply diverse roles in plant development. New Phytol. 177 77–89. PubMed

Rensing K. H. (2002). “Chemical and cryo-fixation for transmission electron microscopy of gymnosperm cambial cells,” in Wood Formation in Trees: Cell and Molecular Biology Techniques, ed. Chaffey N. J. (New York, NY: Taylor and Francis; ), 65–81. 10.1201/9780203166444.ch5 DOI

Savidge R. A. (1988). Auxin and ethylene regulation of diameter growth in trees. Tree Physiol. 4 401–414. 10.1093/treephys/4.4.401 PubMed DOI

Sibout R., Plantegenet S., Hardtke C. S. (2008). Flowering as a condition for xylem expansion in Arabidopsis hypocotyl and root. Curr. Biol. 18 458–463. 10.1016/j.cub.2008.02.070 PubMed DOI

Smetana O., Riikka M., Lyu M., Amiryousefi A., Sánchez Rodríguez F., Wu M. F., et al. (2019). High levels of auxin signalling define the stem cell organiser of the vascular cambium. Nature 565 485–489. 10.1038/s41586-018-0837-0 PubMed DOI

Sundell D., Street N. R., Kumar M., Mellerowicz E. J., Kucukoglu M., Johnsson C., et al. (2017). AspWood: high-spatial-resolution transcriptome profiles reveal uncharacterized modularity of wood formation in Populus tremula. Plant Cell 29 1585–1604. 10.1105/tpc.17.00153 PubMed DOI PMC

Svačinová J., Novák O., Plačková L., Lenobel R., Holík J., Strnad M., et al. (2012). A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods 8:17. 10.1186/1746-4811-8-17 PubMed DOI PMC

Tiimonen H., Häggman H., Tsai C.-J., Chiang V., Aronen T. (2007). The seasonal activity and the effect of mechanical bending and wounding on the PtCOMT promoter in Betula pendula roth. Plant Cell Rep. 26 1205–1214. 10.1007/s00299-007-0331-x PubMed DOI

Tuominen H., Puech L., Fink S., Sundberg B. (1997). A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiol. 115 577–585. 10.1104/pp.115.2.577 PubMed DOI PMC

Vera-Sirera F., De Rybel B., Úrbez C., Kouklas E., Pesquera M., Álvarez-Mahecha J. C., et al. (2015). A bHLH-based feedback loop restricts vascular cell proliferation in plants. Dev. Cell 35 432–443. 10.1016/j.devcel.2015.10.022 PubMed DOI

Vera-Sirera F., Minguet E. G., Singh Kumar S., Ljung K., Tuominen H., Blázquez M. A., et al. (2010). Role of polyamines in plant vascular development. Plant Physiol. Biochem. 48 534–539. 10.1016/j.plaphy.2010.01.011 PubMed DOI

Xu M., Zhang B., Su X., Zhang S., Huang M. (2011). Reference gene selection for quantitative real-time polymerase chain reaction in Populus. Anal. Biochem. 408 337–339. 10.1016/j.ab.2010.08.044 PubMed DOI

Zürcher E., Tavor-Deslex D., Lituiev D., Enkerli K., Tarr P. T., Müller B. (2013). A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiol. 161 1066–1075. 10.1104/pp.112.211763 PubMed DOI PMC

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