Abstract
Nodules are formed as a result of symbiosis with nitrogen-fixing bacteria on the roots of legume plants. Symbiotic nodule development shares common developmental processes with lateral roots, including cell proliferation of the pericycle and cortical cell layers leading to primordium formation, and both these organs are assumed to be evolutionarily related. The progression of their development is realized with the help of phytohormones, in particular auxin and cytokinin. Due to common evolutionary origin, the hormonal pathway and response may have similar functionality in cell fate specification during lateral root and nodule development. It is known that auxin and cytokinin both positively regulate nodule primordia development. However during lateral root development, auxin is a key positive regulator, while cytokinin suppresses lateral root development. Therefore, a comparative review of auxin and cytokinin action in the development of these two organs to elucidate how their identity is established should be of special interest. This review discusses the involvement of auxin and cytokinin in the development of symbiotic nodules and lateral roots, with a special focus on the similarity and differences of their action during lateral root and nodule developmental processes. The spatio-temporal peculiarities of auxin and cytokinin biosynthesis, transport and response during lateral root and symbiotic nodule formation are reviewed, which should help to clarify how the identity of these two root lateral organs depends on auxin-cytokinin interplay.
Graphical Abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen EK, Allen O, Newman A (1953) Pseudonodulation of leguminous plants induced by 2-bromo-3, 5-dichlorobenzoic acid. Am J Bot 40(6):429–435. https://doi.org/10.2307/2438526
Azarakhsh M, Kirienko A, Zhukov V, Lebedeva M, Dolgikh E, Lutova L (2015) KNOTTED1-LIKE HOMEOBOX 3: a new regulator of symbiotic nodule development. J Exp Bot 66(22):7181–7195. https://doi.org/10.1093/jxb/erv414
Azarakhsh M, Lebedeva MA, Lutova LA (2018) Identification and expression analysis of Medicago truncatula isopentenyl transferase genes (IPTs) involved in local and systemic control of nodulation. Front Plant Sci 9:304. https://doi.org/10.3389/fpls.2018.00304
Beeckman T, De Smet I (2014) Pericycle. Curr Biol 24(10):R378–R379. https://doi.org/10.1016/j.cub.2014.03.031
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115(5):591–602. https://doi.org/10.1016/S0092-8674(03)00924-3
Bhalerao RP, Eklöf J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J 29(3):325–332. https://doi.org/10.1046/j.0960-7412.2001.01217.x
Bielach A, Podlešáková K, Marhavý P, Duclercq J, Cuesta C, Müller B, Grunewald W, Tarkowski P, Benková E (2012) Spatiotemporal regulation of lateral root organogenesis in Arabidopsis by cytokinin. Plant Cell 24(10):3967–3981. https://doi.org/10.1105/tpc.112.103044
Bishopp A, Lehesranta S, Vatén A, Help H, El-Showk S, Scheres B, Helariutta K, Mähönen AP, Sakakibara H, Helariutta Y (2011) Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr Biol 21(11):927–932. https://doi.org/10.1016/j.cub.2011.04.049
Boivin S, Fonouni-Farde C, Frugier F (2016) How auxin and cytokinin phytohormones modulate root microbe interactions. Front Plant Sci 7:1240. https://doi.org/10.3389/fpls.2016.01240
Breakspear A, Liu C, Roy S, Stacey N, Rogers C, Trick M, Morieri G, Mysore KS, Wen J, Oldroyd GE (2014) The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26(12):4680–4701. https://doi.org/10.1105/tpc.114.133496
Bustos-Sanmamed P, Mao G, Deng Y, Elouet M, Khan GA, Bazin J, Turner M, Subramanian S, Yu O, Crespi M (2013) Overexpression of miR160 affects root growth and nitrogen-fixing nodule number in Medicago truncatula. Funct Plant Biol 40(12):1208–1220. https://doi.org/10.1071/FP13123
Cao X, Yang H, Shang C, Ma S, Liu L, Cheng J (2019) The roles of auxin biosynthesis YUCCA gene family in plants. Int J Mol Sci 20(24):6343. https://doi.org/10.3390/ijms20246343
Cecchetto G, Amillis S, Diallinas G, Scazzocchio C, Drevet C (2004) The AzgA purine transporter of Aspergillus nidulans: characterization of a protein belonging to a new phylogenetic cluster. J Biol Chem 279(5):3132–3141. https://doi.org/10.1074/jbc.M308826200
Chang L, Ramireddy E, Schmülling T (2015) Cytokinin as a positional cue regulating lateral root spacing in Arabidopsis. J Exp Bot 66(15):4759–4768. https://doi.org/10.1093/jxb/erv252
Chen Z-H, Bao M-L, Sun Y-Z, Yang Y-J, Xu X-H, Wang J-H, Han N, Bian H-W, Zhu M-Y (2011) Regulation of auxin response by miR393-targeted transport inhibitor response protein 1 is involved in normal development in Arabidopsis. Plant Mol Biol 77(6):619–629. https://doi.org/10.1007/s11103-011-9838-1
Chen Y, Chen W, Li X, Jiang H, Wu P, Xia K, Yang Y, Wu G (2014) Knockdown of LjIPT3 influences nodule development in Lotus japonicus. Plant Cell Physiol 55(1):183–193. https://doi.org/10.1093/pcp/pct171
Cho M, Lee SH, Cho H-T (2007) P-Glycoprotein4 displays auxin efflux transporter–like action in Arabidopsis root hair cells and tobacco cells. Plant Cell 19(12):3930–3943. https://doi.org/10.1105/tpc.107.054288
Cooper JB, Long SR (1994) Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6(2):215–225. https://doi.org/10.1105/tpc.6.2.215
D’haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12(6):79R-105R. https://doi.org/10.1093/glycob/12.6.79r
de Billy F, Grosjean C, May S, Bennett M, Cullimore JV (2001) Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol Plant Microbe Interact 14(3):267–277. https://doi.org/10.1094/MPMI.2001.14.3.267
De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D, Van Campenhout J, Overvoorde P, Jansen L, Vanneste S (2010) A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr Biol 20(19):1697–1706. https://doi.org/10.1016/j.cub.2010.09.007
De Smet I, Vanneste S, Inzé D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Mol Biol 60(6):871–887. https://doi.org/10.1007/s11103-005-4547-2
De Smet I, Lau S, Voß U, Vanneste S, Benjamins R, Rademacher EH, Schlereth A, De Rybel B, Vassileva V, Grunewald W (2010) Bimodular auxin response controls organogenesis in Arabidopsis. Proc Natl Acad Sci 107(6):2705–2710. https://doi.org/10.1073/pnas.0915001107
Deinum EE, Kohlen W, Geurts R (2016) Quantitative modelling of legume root nodule primordium induction by a diffusive signal of epidermal origin that inhibits auxin efflux. BMC Plant Biol 16(1):1–14. https://doi.org/10.1186/s12870-016-0935-9
Demchenko K, Demchenko N (2001) Changes of root structure in connection with the development of lateral root primordia in wheat and pumpkins. In: Gašparíková O, Čiamporová M, Mistrík I, Baluška F (eds) Recent advances of plant root structure and function, vol 90. Springer, pp 39–47
Demina IV, Maity PJ, Nagchowdhury A, Ng JL, Van der Graaff E, Demchenko KN, Roitsch T, Mathesius U, Pawlowski K (2019) Accumulation of and response to auxins in roots and nodules of the actinorhizal plant Datisca glomerata compared to the model legume Medicago truncatula. Front Plant Sci 10:1085. https://doi.org/10.3389/fpls.2019.01085
Desbrosses GJ, Stougaard J (2011) Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe 10(4):348–358. https://doi.org/10.1016/j.chom.2011.09.005
Dettmer J, Friml J (2011) Cell polarity in plants: when two do the same, it is not the same. Curr Opin Cell Biol 23(6):686–696. https://doi.org/10.1016/j.ceb.2011.09.006
Dolgikh E, Shaposhnikov A, Dolgikh A, Gribchenko E, Bodyagina K, Yuzhikhin O, Tikhonovich I (2017) Identification of Pisum sativum L cytokinin and auxin metabolic and signaling genes, and an analysis of their role in symbiotic nodule development. Int J Plant Physiol Biochem 9(3):22–35. https://doi.org/10.5897/IJPPB2017.0266
Dubrovsky JG, Rost TL, Colón-Carmona A, Doerner P (2001) Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214(1):30–36. https://doi.org/10.1007/s004250100598
Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benková E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci 105(25):8790–8794. https://doi.org/10.1073/pnas.071230710
Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin YH, Reid DE, Gresshoff PM (2010) Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52(1):61–76. https://doi.org/10.1111/j.1744-7909.2010.00899.x
Fisher J, Gaillard P, Fellbaum CR, Subramanian S, Smith S (2018) Quantitative 3D imaging of cell level auxin and cytokinin response ratios in soybean roots and nodules. Plant, Cell Environ 41(9):2080–2092. https://doi.org/10.1111/pce.13169
Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M (2005) Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J 44(3):382–395. https://doi.org/10.1111/j.1365-313X.2005.02537.x
Gauthier-Coles C, White RG, Mathesius U (2019) Nodulating legumes are distinguished by a sensitivity to cytokinin in the root cortex leading to pseudonodule development. Front Plant Sci 9:1901. https://doi.org/10.3389/fpls.2018.01901
Goto T, Soyano T, Liu M, Mori T & Kawaguchi M (2022) Auxin methylation by IAMT1, duplicated in the legume lineage, promotes root nodule development in Lotus japonicus. Proc Natl Acad Sci 119(10):e2116549119
Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci 105(2):803–808. https://doi.org/10.1073/pnas.0709559105
Goh T, Kasahara H, Mimura T, Kamiya Y, Fukaki H (2012) Multiple AUX/IAA–ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Phil Trans R S B 367(1595):1461–1468. https://doi.org/10.1098/rstb.2011.0232
Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18(10):2680–2693. https://doi.org/10.1105/tpc.106.043778
Guo H-S, Xie Q, Fei J-F, Chua N-H (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17(5):1376–1386. https://doi.org/10.1105/tpc.105.030841
Heckmann AB, Sandal N, Bek AS, Madsen LH, Jurkiewicz A, Nielsen MW, Tirichine L, Stougaard J (2011) Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol Plant Microbe Interact 24(11):1385–1395. https://doi.org/10.1094/MPMI-05-11-0142
Heidstra R, Yang WC, Yalcin Y, Peck S, Emons A, Van Kammen A, Bisseling T (1997) Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction. Development 124(9):1781–1787. https://doi.org/10.1242/dev.124.9.1781
Herrbach V, Remblière C, Gough C, Bensmihen S (2014) Lateral root formation and patterning in Medicago truncatula. J Plant Physiol 171(3–4):301–310. https://doi.org/10.1016/j.jplph.2013.09.006
Hiltenbrand R, Thomas J, McCarthy H, Dykema KJ, Spurr A, Newhart H, Winn ME, Mukherjee A (2016) A developmental and molecular view of formation of auxin-induced nodule-like structures in land plants. Front Plant Sci 7:1692. https://doi.org/10.3389/fpls.2016.01692
Himanen K, Boucheron E, Vanneste S, de Almeida EJ, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14(10):2339–2351. https://doi.org/10.1105/tpc.004960
Hirose N, Takei K, Kuroha T, Kamada-Nobusada T, Hayashi H, Sakakibara H (2008) Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot 59(1):75–83. https://doi.org/10.1093/jxb/erm157
Hirsch A, Bhuvaneswari T, Torrey J, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci 86(4):1244–1248. https://doi.org/10.1073/pnas.86.4.1244
Hobbie L, Estelle M (1995) The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. Plant J 7(2):211–220. https://doi.org/10.1046/j.1365-313x.1995.7020211.x
Hurný A, Cuesta C, Cavallari N, Ötvös K, Duclercq J, Dokládal L, Montesinos JC, Gallemí M, Semerádová H, Rauter T (2020) Synergistic on auxin and cytokinin 1 positively regulates growth and attenuates soil pathogen resistance. Nat Commun 11(1):2170. https://doi.org/10.1038/s41467-020-15895-5
Ioio RD, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17(8):678–682. https://doi.org/10.1016/j.cub.2007.02.047
Ioio RD, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322(5906):1380–1384. https://doi.org/10.1126/science.1164147
Jansen L, Roberts I, De Rycke R, Beeckman T (2012) Phloem-associated auxin response maxima determine radial positioning of lateral roots in maize. Phil Trans R Soc B 367(1595):1525–1533. https://doi.org/10.1098/rstb.2011.0239
Jardinaud M-F, Boivin S, Rodde N, Catrice O, Kisiala A, Lepage A, Moreau S, Roux B, Cottret L, Sallet E (2016) A laser dissection-RNAseq analysis highlights the activation of cytokinin pathways by Nod factors in the Medicago truncatula root epidermis. Plant Physiol 171(3):2256–2276. https://doi.org/10.1104/pp.16.00711
Jarzyniak K, Banasiak J, Jamruszka T, Pawela A, Di Donato M, Novák O, Geisler M, Jasiński M (2021) Early stages of legume–rhizobia symbiosis are controlled by ABCG-mediated transport of active cytokinins. Nature Plants 7(4):428–436. https://doi.org/10.1038/s41477-021-00873-6
Jin J, Watt M, Mathesius U (2012) The autoregulation gene SUNN mediates changes in root organ formation in response to nitrogen through alteration of shoot-to-root auxin transport. Plant Physiol 159(1):489–500. https://doi.org/10.1104/pp.112.194993
Jones B, Gunnerås SA, Petersson SV, Tarkowski P, Graham N, May S, Dolezal K, Sandberg G, Ljung K (2010) Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell 22(9):2956–2969. https://doi.org/10.1105/tpc.110.074856
Kakimoto T (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate: ATP/ADP isopentenyltransferases. Plant Cell Physiol 42(7):677–685. https://doi.org/10.1093/pcp/pce112
Kawata S-i, Shibayama H (1965) On the lateral root primordia formation in the crown roots of rice plants. Jpn J Crop Sci 33(4):423–431. https://doi.org/10.1626/jcs.33.423
Kirolinko C, Hobecker KV, Wen J, Mysore K, Niebel A, Blanco FA, Zanetti ME (2021) Auxin response factor 2 (ARF2), ARF3 and ARF4 mediate both lateral root and nitrogen fixing nodule development in Medicago truncatula. Front Plant Sci 12:465. https://doi.org/10.3389/fpls.2021.659061
Ko D, Kang J, Kiba T, Park J, Kojima M, Do J, Kim KY, Kwon M, Endler A, Song W-Y (2014) Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proc Natl Acad Sci 111(19):7150–7155. https://doi.org/10.1073/pnas.1321519111
Kohlen W, Ng JLP, Deinum EE, Mathesius U (2018) Auxin transport, metabolism, and signalling during nodule initiation: indeterminate and determinate nodules. J Exp Bot 69(2):229–244. https://doi.org/10.1093/jxb/erx308
Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, De Bruijn F (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420(6914):422–426. https://doi.org/10.1038/nature01207
Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J (2007) Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445(7128):652–655. https://doi.org/10.1038/nature05504
Kurepa J, Smalle JA (2022) Auxin/cytokinin antagonistic control of the shoot/root growth ratio and its relevance for adaptation to drought and nutrient deficiency stresses. Int J Mol Sci 23(4):1933. https://doi.org/10.3390/ijms23041933
Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19(12):3889–3900. https://doi.org/10.1105/tpc.107.055863
Lebedeva M, Azarakhsh M, Yashenkova Y, Lutova L (2020) Nitrate-induced CLE peptide systemically inhibits nodulation in Medicago truncatula. Plants 9(11):1456. https://doi.org/10.3390/plants9111456
Lebedeva M, Azarakhsh M, Sadikova D, Lutova L (2021) At the root of nodule organogenesis: conserved regulatory pathways recruited by rhizobia. Plants 10(12):2654. https://doi.org/10.3390/plants10122654
Lee B-h, Johnston R, Yang Y, Gallavotti A, Kojima M, Travençolo BA, Costa LdF, Sakakibara H, Jackson D (2009) Studies of aberrant phyllotaxy1 mutants of maize indicate complex interactions between auxin and cytokinin signaling in the shoot apical meristem. Plant Physiol 150(1):205–216. https://doi.org/10.1104/pp.109.137034
Lee HJ, Kim HS, Park JM, Cho HS, Jeon JH (2020) PIN-mediated polar auxin transport facilitates root—obstacle avoidance. New Phytol 225(3):1285–1296. https://doi.org/10.1111/nph.16076
Li X, Mo X, Shou H, Wu P (2006) Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis. Plant Cell Physiol 47(8):1112–1123. https://doi.org/10.1093/pcp/pcj082
Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PloS One 7(11):e48951. https://doi.org/10.1371/journal.pone.0048951
Libbenga K, Harkes P (1973) Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L. Planta 114(1):17–28. https://doi.org/10.1007/BF00390281
Lin J, Roswanjaya YP, Kohlen W, Stougaard J, Reid D (2021) Nitrate restricts nodule organogenesis through inhibition of cytokinin biosynthesis in Lotus japonicus. Nat Commun 12(1):1–12. https://doi.org/10.1038/s41467-021-26820-9
Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Gr S (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17(4):1090–1104. https://doi.org/10.1105/tpc.104.029272
Luo J, Zhou J-J, Zhang J-Z (2018) Aux/IAA gene family in plants: molecular structure, regulation, and function. Int J Mol Sci 19(1):259. https://doi.org/10.3390/ijms19010259
Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis auxin response factor17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17(5):1360–1375. https://doi.org/10.1105/tpc.105.031716
Mansfield TA, Schultes NP, Mourad GS (2009) AtAzg1 and AtAzg2 comprise a novel family of purine transporters in Arabidopsis. FEBS Lett 583(2):481–486. https://doi.org/10.1016/j.febslet.2008.12.048
Mao G, Turner M, Yu O, Subramanian S (2013) miR393 and miR164 influence indeterminate but not determinate nodule development. Plant Signal Behav 8(10):e26753. https://doi.org/10.4161/psb.26753
Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14(3):589–597. https://doi.org/10.1105/tpc.010354
Marhavý P, Bielach A, Abas L, Abuzeineh A, Duclercq J, Tanaka H, Pařezová M, Petrášek J, Friml J, Kleine-Vehn J (2011) Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev Cell 21(4):796–804. https://doi.org/10.1016/j.devcel.2011.08.014
Marhavý P, Vanstraelen M, De Rybel B, Zhaojun D, Bennett MJ, Beeckman T, Benková E (2013) Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J 32(1):149–158. https://doi.org/10.1038/emboj.2012.303
Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci 108(45):18512–18517. https://doi.org/10.1073/pnas.1108434108
Mathesius U (2008) Goldacre paper: auxin: at the root of nodule development? Funct Plant Biol 35(8):651–668. https://doi.org/10.1071/FP08177
Mathesius U, Schlaman HR, Spaink HP, Of Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14(1):23–34. https://doi.org/10.1046/j.1365-313X.1998.00090.x
Mathesius U, Weinman JJ, Rolfe BG, Djordjevic MA (2000) Rhizobia can induce nodules in white clover by “hijacking” mature cortical cells activated during lateral root development. Mol Plant Microbe Interact 13(2):170–182. https://doi.org/10.1094/MPMI.2000.13.2.170
Mens C, Li D, Haaima LE, Gresshoff PM, Ferguson BJ (2018) Local and systemic effect of cytokinins on soybean nodulation and regulation of their isopentenyl transferase (IPT) biosynthesis genes following rhizobia inoculation. Front Plant Sci 9:1150. https://doi.org/10.3389/fpls.2018.01150
Mens C, Hastwell AH, Su H, Gresshoff PM, Mathesius U, Ferguson BJ (2021) Characterisation of Medicago truncatula CLE34 and CLE35 in nitrate and rhizobia regulation of nodulation. New Phytol 229(5):2525–2534. https://doi.org/10.1111/nph.17010
Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37(1):128–138. https://doi.org/10.1046/j.1365-313x.2003.01945.x
Moreau C, Gautrat P, Frugier F (2021) Nitrate-induced CLE35 signaling peptides inhibit nodulation through the SUNN receptor and miR2111 repression. Plant Physiol 185(3):1216–1228. https://doi.org/10.1093/plphys/kiaa094
Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, D’haeseleer K, Holsters M, Goormachtig S (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153(1):222–237. https://doi.org/10.1104/pp.110.153718
Mortier V, Wasson A, Jaworek P, De Keyser A, Decroos M, Holsters M, Tarkowski P, Mathesius U, Goormachtig S (2014) Role of LONELY GUY genes in indeterminate nodulation on Medicago truncatula. New Phytol 202(2):582–593. https://doi.org/10.1111/nph.12681
Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315(5808):101–104. https://doi.org/10.1126/science.1132514
Nadzieja M, Kelly S, Stougaard J, Reid D (2018) Epidermal auxin biosynthesis facilitates rhizobial infection in Lotus japonicus. Plant J 95(1):101–111. https://doi.org/10.1111/tpj.13934
Nadzieja M, Stougaard J, Reid D (2019) A toolkit for high resolution imaging of cell division and phytohormone signaling in legume roots and root nodules. Front Plant Sci 10:1000. https://doi.org/10.3389/fpls.2019.01000
Ng JL, Mathesius U (2018) Acropetal auxin transport inhibition is involved in indeterminate but not determinate nodule formation. Front Plant Sci 9:169. https://doi.org/10.3389/fpls.2018.00169
Ng JL, Welvaert A, Wen J, Chen R, & Mathesius U (2020) The Medicago truncatula PIN2 auxin transporter mediates basipetal auxin transport but is not necessary for nodulation. J Exp Bot 71(4):1562–1573
Ng JLP, Hassan S, Truong TT, Hocart CH, Laffont C, Frugier F, Mathesius U (2015) Flavonoids and auxin transport inhibitors rescue symbiotic nodulation in the Medicago truncatula cytokinin perception mutant cre1. Plant Cell 27(8):2210–2226. https://doi.org/10.1105/tpc.15.00231
Nishimura R, Ohmori M, Fujita H, Kawaguchi M (2002) A Lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulation. Proc Natl Acad Sci 99(23):15206–15210. https://doi.org/10.1073/pnas.222302699
Nordström A, Tarkowski P, Tarkowska D, Norbaek R, Åstot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin–cytokinin-regulated development. Proc Natl Acad Sci 101(21):8039–8044. https://doi.org/10.1073/pnas.0402504101
Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50(1):67–77. https://doi.org/10.1093/pcp/pcn194
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19(1):118–130. https://doi.org/10.1105/tpc.106.047761
Op den Camp RH, De Mita S, Lillo A, Cao Q, Limpens E, Bisseling T, Geurts R (2011) A phylogenetic strategy based on a legume-specific whole genome duplication yields symbiotic cytokinin type-A response regulators. Plant Physiol 157(4):2013–2022. https://doi.org/10.1104/pp.111.187526
Osugi A, Sakakibara H (2015) Q&A: How do plants respond to cytokinins and what is their importance? BMC Biol 13(1):1–10. https://doi.org/10.1186/s12915-015-0214-5
Penmetsa RV, Frugoli JA, Smith LS, Long SR, Cook DR (2003) Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol 131(3):998–1008. https://doi.org/10.1104/pp.015677
Plet J, Wasson A, Ariel F, Le Signor C, Baker D, Mathesius U, Crespi M, Frugier F (2011) MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J 65(4):622–633. https://doi.org/10.1111/j.1365-313X.2010.04447.x
Reid DE, Ferguson BJ, Gresshoff PM (2011) Inoculation-and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant Microbe Interact 24(5):606–618. https://doi.org/10.1094/MPMI-09-10-0207
Reid DE, Heckmann AB, Novák O, Kelly S, Stougaard J (2016) Cytokinin oxidase/dehydrogenase3 maintains cytokinin homeostasis during root and nodule development in Lotus japonicus. Plant Physiol 170(2):1060–1074. https://doi.org/10.1104/pp.15.00650
Reid D, Nadzieja M, Novák O, Heckmann AB, Sandal N, Stougaard J (2017) Cytokinin biosynthesis promotes cortical cell responses during nodule development. Plant Physiol 175(1):361–375. https://doi.org/10.1104/pp.17.00832
Riefler M, Novak O, Strnad M, Schmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18(1):40–54. https://doi.org/10.1105/tpc.105.037796
Rightmyer AP, Long SR (2011) Pseudonodule formation by wild-type and symbiotic mutant Medicago truncatula in response to auxin transport inhibitors. Mol Plant Microbe Interact 24(11):1372–1384. https://doi.org/10.1094/MPMI-04-11-0103
Roudier F, Fedorova E, Lebris M, Lecomte P, Györgyey J, Vaubert D, Horvath G, Abad P, Kondorosi A, Kondorosi E (2003) The Medicago species A2-type cyclin is auxin regulated and involved in meristem formation but dispensable for endoreduplication-associated developmental programs. Plant Physiol 131(3):1091–1103. https://doi.org/10.1104/pp.102.011122
Roy S, Robson F, Lilley J, Liu C-W, Cheng X, Wen J, Walker S, Sun J, Cousins D, Bone C (2017) MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis. Plant Physiol 174(1):326–338. https://doi.org/10.1104/pp.16.01473
Sańko-Sawczenko I, Łotocka B, Czarnocka W (2016) Expression analysis of PIN genes in root tips and nodules of Medicago truncatula. Int J Mol Sci 17(8):1197. https://doi.org/10.3390/ijms17081197
Sasaki T, Suzaki T, Soyano T, Kojima M, Sakakibara H, Kawaguchi M (2014) Shoot-derived cytokinins systemically regulate root nodulation. Nat Commun 5(1):1–9. https://doi.org/10.1038/ncomms5983
Scheres B, McKhann HI, Zalensky A, Löbler M, Bisseling T, Hirsch AM (1992) The PsENOD12 gene is expressed at two different sites in Afghanistan pea pseudonodules induced by auxin transport inhibitors. Plant Physiol 100(4):1649–1655. https://doi.org/10.1104/pp.100.4.1649
Schiessl K, Lilley JL, Lee T, Tamvakis I, Kohlen W, Bailey PC, Thomas A, Luptak J, Ramakrishnan K, Carpenter MD (2019) NODULE INCEPTION recruits the lateral root developmental program for symbiotic nodule organogenesis in Medicago truncatula. Curr Biol 29(21):3657–3668. https://doi.org/10.1016/j.cub.2019.09.005
Schlereth A, Möller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jürgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464(7290):913–916. https://doi.org/10.1038/nature08836
Schnabel E, Journet E-P, de Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 58(6):809–822. https://doi.org/10.1007/s11103-005-8102-y
Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299(5603):109–112. https://doi.org/10.1126/science.1077937
Shen C, Yue R, Yang Y, Zhang L, Sun T, Xu L, Tie S, Wang H (2014) Genome-wide identification and expression profiling analysis of the Aux/IAA gene family in Medicago truncatula during the early phase of Sinorhizobium meliloti infection. PLoS One 9(9):e107495. https://doi.org/10.1371/journal.pone.0107495
Shkolnik-Inbar D, Bar-Zvi D (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell 22(11):3560–3573. https://doi.org/10.1105/tpc.110.074641
Soyano T, Liu M, Kawaguchi M, Hayashi M (2021) Leguminous nodule symbiosis involves recruitment of factors contributing to lateral root development. Curr Opin Plant Biol 59:102000. https://doi.org/10.1016/j.pbi.2020.102000
Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie D-Y, Doležal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133(1):177–191. https://doi.org/10.1016/j.cell.2008.01.047
Su Y-H, Liu Y-B, Zhang X-S (2011) Auxin–cytokinin interaction regulates meristem development. Mol Plant 4(4):616–625. https://doi.org/10.1093/mp/ssr007
Suzaki T, Yano K, Ito M, Umehara Y, Suganuma N, Kawaguchi M (2012) Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 139(21):3997–4006. https://doi.org/10.1242/dev.084079
Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10(8):946–954. https://doi.org/10.1038/ncb1754
Takanashi K, Sugiyama A, Yazaki K (2011) Involvement of auxin distribution in root nodule development of Lotus japonicus. Planta 234(1):73–81. https://doi.org/10.1007/s00425-011-1385-0
Takei K, Sakakibara H, Sugiyama T (2001) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, inArabidopsis thaliana. J Biol Chem 276(28):26405–26410. https://doi.org/10.1074/jbc.M102130200
Takei K, Yamaya T, Sakakibara H (2004) Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-zeatin. J Biol Chem 279(40):41866–41872. https://doi.org/10.1074/jbc.M406337200
Tessi TM, Brumm S, Winklbauer E, Schumacher B, Pettinari G, Lescano I, González CA, Wanke D, Maurino VG, Harter K (2021) Arabidopsis AZG2 transports cytokinins in vivo and regulates lateral root emergence. New Phytol 229(2):979–993. https://doi.org/10.1111/nph.16943
Timmers A, Auriac M-C, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126(16):3617–3628. https://doi.org/10.1242/dev.126.16.3617
Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315(5808):104–107. https://doi.org/10.1126/science.1132397
Triozzi PM, Irving TB, Schmidt HW, Keyser ZP, Chakraborty S, Balmant K, Pereira WJ, Dervinis C, Mysore KS, Wen J (2022) Spatiotemporal cytokinin response imaging and ISOPENTENYLTRANSFERASE 3 function in Medicago nodule development. Plant Physiol 188(1):560–575. https://doi.org/10.1093/plphys/kiab447
Turner M, Nizampatnam NR, Baron M, Coppin S, Damodaran S, Adhikari S, Arunachalam SP, Yu O, Subramanian S (2013) Ectopic expression of miR160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean. Plant Physiol 162(4):2042–2055. https://doi.org/10.1104/pp.113.220699
van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U (2006) Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiol 140(4):1494–1506. https://doi.org/10.1104/pp.105.075879
Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28:463–487. https://doi.org/10.1146/annurev-cellbio-101011-155741
Vanneste S, De Rybel B, Beemster GT, Ljung K, De Smet I, Van Isterdael G, ... & Beeckman T (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14- mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17(11):3035–3050
Vernié T, Kim J, Frances L, Ding Y, Sun J, Guan D, Niebel A, Gifford ML, de Carvalho-Niebel F, Oldroyd GE (2015) The NIN transcription factor coordinates diverse nodulation programs in different tissues of the Medicago truncatula root. Plant Cell 27(12):3410–3424. https://doi.org/10.1105/tpc.15.00461
Wang J-W, Wang L-J, Mao Y-B, Cai W-J, Xue H-W, Chen X-Y (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17(8):2204–2216. https://doi.org/10.1105/tpc.105.033076
Wang Y, Li K, Chen L, Zou Y, Liu H, Tian Y, Li D, Wang R, Zhao F, Ferguson BJ (2015) MicroRNA167-directed regulation of the auxin response factors GmARF8a and GmARF8b is required for soybean nodulation and lateral root development. Plant Physiol 168(3):984–999. https://doi.org/10.1104/pp.15.00265
Wang Y, Yang W, Zuo Y, Zhu L, Hastwell AH, Chen L, Tian Y, Su C, Ferguson BJ, Li X (2019) GmYUC2a mediates auxin biosynthesis during root development and nodulation in soybean. J Exp Bot 70(12):3165–3176. https://doi.org/10.1093/jxb/erz144
Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12(5):527–538. https://doi.org/10.1016/j.pbi.2009.07.002
Werner Ts, 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. Plant Cell 15(11):2532–2550. https://doi.org/10.1105/tpc.014928
Werner T, Köllmer I, Bartrina I, Holst K, Schmülling T (2006) New insights into the biology of cytokinin degradation. Plant Biol 8(03):371–381. https://doi.org/10.1055/s-2006-923928
Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y (2011) Conversion of tryptophan to indole-3-acetic acid by tryptophan aminotransferases of Arabidopsis and yuccas in Arabidopsis. Proc Natl Acad Sci 108(45):18518–18523. https://doi.org/10.1073/pnas.1108436108
Xiao TT, Schilderink S, Moling S, Deinum EE, Kondorosi E, Franssen H, Kulikova O, Niebel A, Bisseling T (2014) Fate map of Medicago truncatula root nodules. Development 141(18):3517–3528. https://doi.org/10.1242/dev.110775
Xiao TT, van Velzen R, Kulikova O, Franken C, Bisseling T (2019) Lateral root formation involving cell division in both pericycle, cortex and endodermis is a common and ancestral trait in seed plants. Development 146(20):dev182592. https://doi.org/10.1242/dev.182592
Xu C, Cao H, Xu E, Zhang S, Hu Y (2018) Genome-wide identification of Arabidopsis LBD29 target genes reveals the molecular events behind auxin-induced cell reprogramming during callus formation. Plant Cell Physiol 59(4):749–760. https://doi.org/10.1093/pcp/pcx168
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63(4):968–989. https://doi.org/10.1128/MMBR.63.4.968-989.1999
Zhang W, Swarup R, Bennett M, Schaller GE, Kieber JJ (2013) Cytokinin induces cell division in the quiescent center of the Arabidopsis root apical meristem. Curr Biol 23(20):1979–1989. https://doi.org/10.1016/j.cub.2013.08.008
Zürcher E, Tavor-Deslex D, Lituiev D, Enkerli K, Tarr PT, Müller B (2013) A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiol 161(3):1066–1075. https://doi.org/10.1104/pp.112.211763
Zürcher E, Liu J, di Donato M, Geisler M, Müller B (2016) Plant development regulated by cytokinin sinks. Science 353(6303):1027–1030. https://doi.org/10.1126/science.aaf7254
Funding
This work was supported by the Center for International Scientific Studies & Collaborations (CISSC), Ministry of Science Research and Technology of Iran, and Saint-Petersburg State University Grant ID: 93020341 provided to Maria Lebedeva.
Author information
Authors and Affiliations
Contributions
The conceptualization of the theme, literature search and data analysis, original draft preparation: MA; review and editing: MA and ML. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Handling Editor: Francesca Resentini.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Azarakhsh, M., Lebedeva, M.A. Lateral Root versus Nodule: The Auxin-Cytokinin Interplay. J Plant Growth Regul 42, 6903–6919 (2023). https://doi.org/10.1007/s00344-023-10983-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-023-10983-4