Cytokinins regulate root growth through its action on meristematic cell proliferation but not on the transition to differentiation
Victor B. Ivanov A C and Alexey N. Filin A B
+ Author Affiliations
- Author Affiliations
A Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya str. 35, 127276, Moscow, Russia.
B Moscow State University, Faculty of Biology, Botanical Garden, Leninskie Gory1 (12), 119991, Moscow, Russia.
C Corresponding author. Email: ivanov_vb@mail.ru
This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 19–23 June 2016.
Functional Plant Biology 45(2) 215-221 https://doi.org/10.1071/FP16340
Submitted: 30 September 2016 Accepted: 1 February 2017 Published: 28 March 2017
Abstract
Contrary to the wide-spread view that cytokinins change the rate of root growth and meristem size by regulating the cell transition to elongation (differentiation), our data showed that cytokinins affected the cell cycle duration in the meristem. The rate of meristematic cell transition to elongation itself is regulated by two groups of independent processes, through influence on (i) the life-span of cells in the meristem, and (ii) the cell proliferation rate in the meristem. Trans-zeatin slows down the root growth rate and the cell transition to elongation as a result of prolongation of mitotic cycles. The life-span of cells in the meristem does not change. The number of meristematic cells in one file decreases due to inhibition of cell proliferation but not to an acceleration of cell transition to elongation. Roots of triple mutant ipt3ipt5ipt7, in which cytokinin synthesis is slowed down, behave in an opposite way such that the rate of cell transition to elongation and cell proliferation is speeded up. Their peculiarity is that the life-span of cells in meristem becomes shorter than in control roots. In both cases, a change in concentration of endogenous cytokinin or in its signalling are associated with a change in mitotic cycle duration.
Additional keywords: Arabidopsis thaliana, cell transition to differentiation, cytokinin, mitotic cycle, root apical meristem, root cell growth.
References
Baluška F, Mancuso S, Volkmann D, Barlow PW (2010) Root apex transition zone: a signalling-response nexus in the root. Trends in Plant Science 15, 402–408.| Root apex transition zone: a signalling-response nexus in the root.Crossref | GoogleScholarGoogle Scholar |
Beemster GTS, Baskin TI (2000) STUNTED PLANT 1 mediates effects of cytokinin, but not of auxin, on cell and expansion in the root of Arabidopsis. Plant Physiology 124, 1718–1727.
| STUNTED PLANT 1 mediates effects of cytokinin, but not of auxin, on cell and expansion in the root of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitVWrsg%3D%3D&md5=6938bcb58b5dde57da4c421e6f989edcCAS |
Benková E, Hejátko J (2009) Hormone interactions at the root apical meristem. Plant Molecular Biology 69, 383–396.
| Hormone interactions at the root apical meristem.Crossref | GoogleScholarGoogle Scholar |
Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39–44.
| The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovFCj&md5=6f1189571f88806ab4eb8bb2dcb4c88bCAS |
Colon-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Technical advances: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. The Plant Journal 20, 503–508.
| Technical advances: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksVOgsg%3D%3D&md5=c54b8a1e2919caef733006b2f31a2504CAS |
Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Current Biology 17, 678–682.
| Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkt1ahsLk%3D&md5=667263c354d583cf9a1538e6180cb5ddCAS |
Dubrovsky JG, Soukup A, Napsucialy-Mendivil S, Jeknic Z, Ivanchenko MG (2009) The lateral root initiation index: an integrative measure of primordium formation. Annals of Botany 103, 807–817.
| The lateral root initiation index: an integrative measure of primordium formation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M7kslOhtg%3D%3D&md5=0684ea2367f2ab1e578f2c8d9acd28f7CAS |
Federici F, Dupuy L, Laplaze L, Heisler M, Haseloff J (2012) Integrated genetic and computation methods for in planta cytometry. Nature Methods 9, 483–485.
| Integrated genetic and computation methods for in planta cytometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvVGqsLw%3D&md5=d60eab07486aa9ff09b5b97677476dbdCAS |
Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Current Opinion in Plant Biology 8, 518–525.
| Cytokinin signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXosVahtr4%3D&md5=d56fa44f679110468e8f2a8d3def226dCAS |
Filin AN, Ivanov VB (2016) Effect of 2,4 D on cell proliferation and elongation in the roots of Arabidopsis thaliana. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 63, 166–171.
| Effect of 2,4 D on cell proliferation and elongation in the roots of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XisFOksLc%3D&md5=01cb5dccd0247ba18524850ff7727acdCAS |
Grif VG, Ivanov VB, Machs EM (2002) Cell cycle and its parameters in flowering plants. Cytologia 44, 936–980.
Higuchi M, Pischke MS, Manonen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta Y, Sussman MR, Kakimoto T (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proceedings of the National Academy of Sciences of the United States of America 101, 8821–8826.
| In planta functions of the Arabidopsis cytokinin receptor family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKkt78%3D&md5=dfe962f7357e9a0819c15f1dedbf8fd8CAS |
Ivanov VB (1994) Root growth responses to chemicals. Soviet scientific reviews. D 13, 1–70.
Ivanov VB, Dubrovsky JG (1997) Estimation of the cell-cycle duration in the root apical meristem: a model of linkage between cell-cycle duration, rate of cell production, and rate of root growth. International Journal of Plant Sciences 158, 757–763.
| Estimation of the cell-cycle duration in the root apical meristem: a model of linkage between cell-cycle duration, rate of cell production, and rate of root growth.Crossref | GoogleScholarGoogle Scholar |
Ivanov VB, Dubrovsky J (2013) Longitudinal zonation pattern in plant roots: conflicts and solutions. Trends in Plant Science 18, 237–243.
| Longitudinal zonation pattern in plant roots: conflicts and solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1ajt7fL&md5=753e624ddc641e402bbb1b553184883fCAS |
Kagenishi T, Yokawa K, Baluška F (2016) MES buffer affects Arabidopsis root apex zonation and root growth by suppressing superoxide generation in root apex. Frontiers in Plant Science 7, 79
| MES buffer affects Arabidopsis root apex zonation and root growth by suppressing superoxide generation in root apex.Crossref | GoogleScholarGoogle Scholar |
Kato R, Shimoyama T, Takagi K, Suzuki T (1995) Effects of cytokinins on the growth of primary roots of Zea mays. Plant & Cell Physiology 36, 1477–1482.
Kieber JJ, Schaller GE (2014) Cytokinins. The Arabidopsis Book/American Society of Plant Biologists 12, e0168
| Cytokinins.Crossref | GoogleScholarGoogle Scholar |
Kinoshita A, ten Hove CA, Tabata R, Yamada M, Shimizu N, Ishida T, Yamaguchi K, Shigenobu S, Takebayashi Y, Luchi S, Kobayashi M, Kurata T, Wada T, Seo M, Hasebe M, Blilou I, Fukuda H, Scheres B, Heidstra R, Kamiya Y, Sawa S (2015) A plant U-box protein, PUB4, regulates asymmetric cell division and cell proliferation in the root meristem. Development 142, 444–453.
| A plant U-box protein, PUB4, regulates asymmetric cell division and cell proliferation in the root meristem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmtlSjsr8%3D&md5=b14a140a8da3f413be282fe62693df2eCAS |
Kuderová A, Urbánková I, Válková M, Malbeck J, Brzobohatý B, Némethová D, Hejátko J (2008) Effects of conditional IPT-dependent cytokinin overproduction on root architecture of Arabidopsis seedlings. Plant & Cell Physiology 49, 470–482.
| Effects of conditional IPT-dependent cytokinin overproduction on root architecture of Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar |
López-Bucio JS, Dubrovsky JG, Raya-González J, Ugartechea-Chirino Y, López-Bucio J, de Luna-Valdez LA, Ramos-Vega M, León P, Guevara-García AA (2014) Arabidopsis thaliana mitogen-activated protein kinase 6 is involved in seed formation and modulation of primary and lateral root development. Journal of Experimental Botany 65, 169–183.
| Arabidopsis thaliana mitogen-activated protein kinase 6 is involved in seed formation and modulation of primary and lateral root development.Crossref | GoogleScholarGoogle Scholar |
Mancuso S, Marras AM, Magnus V, Baluška F (2005) Non-invasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode. Analytical Biochemistry 341, 344–351.
| Non-invasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktleisr8%3D&md5=ca55084296ff571103bd64dad883e1f6CAS |
Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annual Review of Plant Physiology and Plant Molecular Biology 52, 89–118.
| Cytokinin metabolism and action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWgsL8%3D&md5=b0030b3de62182a8b38e1d3e6c3c9c58CAS |
Napsucialy-Mendivil S, Alvarez-Venegas R, Shishkova S, Dubrovsky JG (2014) ARABIDOPSIS HOMOLOG of TRITHORAX1 (ATX1) is required for cell production, patterning, and morphogenesis in root development. Journal of Experimental Botany 65, 6373–6384.
| ARABIDOPSIS HOMOLOG of TRITHORAX1 (ATX1) is required for cell production, patterning, and morphogenesis in root development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1Gis73J&md5=cc0bf63f9943689e7e2403954366a2adCAS |
Peng Y, Ma W, Chen L, Yang L, Li S, Zhao H, Zhao Y, Jin W, Li N, Bevan MW, Li X, Tong Y, Li Y (2013) Control of root meristem size by DA1-RELATED PROTEIN2 in Arabidopsis. Plant Physiology 161, 1542–1556.
| Control of root meristem size by DA1-RELATED PROTEIN2 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvFKru7k%3D&md5=5f342ffa90b135cb785e09c9c663ccc7CAS |
Rodriguez RE, Ercoli MF, Debernardi JM, Breakfield NW, Mecchia MA, Sabatini M, Cools T, De Veylder L, Benfey PN, Palatnik JF (2015) MicroRNA miR396 regulates the switch between stem cells and transit-amplifying cells in Arabidopsis roots. The Plant Cell 27, 3354–3366.
| MicroRNA miR396 regulates the switch between stem cells and transit-amplifying cells in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtlyiurzF&md5=88dfe2dbd837fd324526f31f3c15231aCAS |
Schaller GE, Street JH, Kieber JJ (2014) Cytokinin and cell cycle. Current Opinion in Plant Biology 21, 7–15.
| Cytokinin and cell cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1ensbfE&md5=b51d06ece49948aea7f79a0061f995b2CAS |
Šimášková M, O’Brien JA, Khan M, Van Noorden G, Ötvös K, Vieten A, De Clercq I, Van Haperen JM, Cuesta C, Hoyerová K, Vanneste S, Marhavý P, Wabnik K, Van Breusegem F, Nowack M, Murphy A, Friml J, Weijers D, Beeckman T, Benková E (2015) Cytokinin response factors regulate PIN-FORMED auxin transporters. Nature Communications 6, 8717
| Cytokinin response factors regulate PIN-FORMED auxin transporters.Crossref | GoogleScholarGoogle Scholar |
Skylar A, Wu X (2011) Regulation of meristem size by cytokinin signaling. Journal of Integrative Plant Biology 53, 446–454.
| Regulation of meristem size by cytokinin signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptlWrsL8%3D&md5=e830efab4853ee880ee38381155d2d87CAS |
Takahashi N, Kajihara T, Okamura C, Kim Y, Katagiri Y, Okushima Y, Matsunaga S, Hwang I, Umeda M (2013) Cytokinins control endocycle onset by promoting the expression of an APC/C activator in Arabidopsis roots. Current Biology 23, 1812–1817.
| Cytokinins control endocycle onset by promoting the expression of an APC/C activator in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVCltLfN&md5=71f7d8ffa493a99b913d711579bb5711CAS |
Verbelen JP, De Cnodder T, Le J, Vissenberg K, Baluška F (2006) The root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: meristematic zone, transition zone, fast elongation zone and growth terminating zone. Plant Signaling & Behavior 1, 296–304.
| The root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: meristematic zone, transition zone, fast elongation zone and growth terminating zone.Crossref | GoogleScholarGoogle Scholar |
Webster PL, MacLeod RD (1980) Characteristics of root apical meristem cell population kinetics: a review of analyses and concepts. Environmental and Experimental Botany 20, 335–358.
| Characteristics of root apical meristem cell population kinetics: a review of analyses and concepts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtFGquw%3D%3D&md5=4275f17bc9cf1b5cf480cb1f7132a3a7CAS |
Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. The Plant Cell 15, 2532–2550.
| Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1Ortbw%3D&md5=8a547f40c5ec492875f69aea29c3d747CAS |
