Abstract
SymRK-interacting protein 1 (SIP1) has previously been shown to interact with the symbiosis receptor kinase, SymRK, in Lotus japonicus. A longer variant of the SIP1 transcript, SIP1L, was isolated and characterized. SIP1L contains an additional 17 amino acids that make its C-terminus a complete heat shock protein 20 (Hsp20)-like domain. In contrast to SIP1S, the longer splicing variant SIP1L could not interact with SymRK. Both SIP1L and SIP1S transcripts could be detected in developing nodules and other plant tissues, although the former was always more abundant than the latter. SIP1L and SIP1S formed heteromeric protein complexes, which were co-localized in the plasma membrane, cytoplasm and nuclei. Expression of SIP1-RNAi in transgenic hairy roots resulted in impairment in the nodule and arbuscular mycorrhizal development, suggesting an important role of SIP1 in the common symbiosis pathway. Overexpression of either SIP1L or SIP1S increased the number of nodules formed on transgenic hairy roots, indicating a positive role of SIP1 in nodulation. The SIP1S-like transcript was not detected in other higher plants tested, and the SIP1L-like proteins of these plants were capable of interacting with the SymRK orthologs. It is proposed that the loss of the ability of SIP1L to interact with SymRK in Lotus is compensated by the expression of a shorter splicing variant, SIP1S, which binds SymRK and may play a role in relaying the symbiosis signals to downstream cellular events.
Similar content being viewed by others
References
Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker DG, de Carvalho-Niebel F (2007) AP2-ERF transcription factors mediate Nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19:2866–2885
Ane JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Levy J, Debelle F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Denarie J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367
Basha E, Lee GJ, Demeler B, Vierling E (2004) Chaperone activity of cytosolic small heat shock proteins from wheat. Eur J Biochem 271:1426–1436
Brewin NJ (1991) Development of the legume root nodule. Annu Rev Cell Biol 7:191–226
Broughton WJ, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125:1075–1080
Charpentier M, Bredemeier R, Wanner G, Takeda N, Schleiff E, Parniske M (2008) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20:3467–3479
Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernie T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20:3084–3088
Combier JP, de Billy F, Gamas P, Niebel A, Rivas S (2008) Trans-regulation of the expression of the transcription factor MtHAP2-1 by a uORF controls root nodule development. Genes Dev 22:1549–1559
Dallas PB, Pacchione S, Wilsker D, Bowrin V, Kobayashi R, Moran E (2000) The human SWI-SNF complex protein p270 is an ARID family member with non-sequence-specific DNA binding activity. Mol Cell Biol 20:3137–3146
D’Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79R–105R
Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966
Garcia-Ranea JA, Mirey G, Camonis J, Valencia A (2002) p23 and HSP20/alpha-crystallin proteins define a conserved sequence domain present in other eukaryotic protein families. FEBS Lett 529:162–167
Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499
Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P (2008) Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20:1407–1420
Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Peret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc Natl Acad Sci USA 105:4928–4932
Gough C, Cullimore J (2011) Lipo-chitooligosaccharide signalling in endosymbiotic plant-microbe interactions. Mol Plant Microbe Interact 24:867–878
Gregory SL, Kortschak RD, Kalionis B, Saint R (1996) Characterization of the dead ringer gene identifies a novel, highly conserved family of sequence-specific DNA-binding proteins. Mol Cell Biol 16:792–799
Groth M, Takeda N, Perry J, Uchida H, Draxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang TL, Parniske M (2010) NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22:2509–2526
Heckmann AB, Lombardo F, Miwa H, Perry JA, Bunnewell S, Parniske M, Wang TL, Downie JA (2006) Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol 142:1739–1750
Herrscher RF, Kaplan MH, Lelsz DL, Das C, Scheuermann R, Tucker PW (1995) The immunoglobulin heavy-chain matrix-associating regions are bound by Bright: a B cell-specific trans-activator that describes a new DNA-binding protein family. Genes Dev 9:3067–3082
Hirsch S, Kim J, Munoz A, Heckmann AB, Downie JA, Oldroyd GE (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21:545–557
Imaizumi-Anraku H, Kouchi H, Syono K, Akao S, Kawaguchi M (2000) Analysis of ENOD40 expression in alb1, a symbiotic mutant of Lotus japonicus that forms empty nodules with incompletely developed nodule vascular bundles. Mol Gen Genet 264:402–410
Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie JA, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:527–531
Kalo P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GE (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308:1786–1789
Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103:359–364
Kang H, Zhu H, Chu X, Yang Z, Yuan S, Yu D, Wang C, Hong Z, Zhang Z (2011) A novel interaction between CCaMK and a protein containing the Scythe_N ubiquitin-like domain in Lotus japonicus. Plant Physiol 155:1312–1324
Kumagai H, Kouchi H (2003) Gene silencing by expression of hairpin RNA in Lotus japonicus roots and root nodules. Mol Plant Microbe Interact 16:663–668
Kumar T, Majumdar A, Das P, Sarafis V, Ghose M (2008) Trypan blue as a fluorochrome for confocal laser scanning microscopy of arbuscular mycorrhizae in three mangroves. Biotech Histochem 83:153–159
Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome JC, Denarie J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784
Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C, Debelle F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364
Libault M, Joshi T, Benedito VA, Xu D, Udvardi MK, Stacey G (2009) Legume transcription factor genes: what makes legumes so special? Plant Physiol 151:991–1001
Limpens E, Ramos J, Franken C, Raz V, Compaan B, Franssen H, Bisseling T, Geurts R (2004) RNA interference in Agrobacterium rhizogenes-transformed roots of Arabidopsis and Medicago truncatula. J Exp Bot 55:983–992
Lotocka B (2008) Vascular system within developing root nodules of Lupinus luteus L. Part 1. Juvenile stage. Acta Biol Cracov Bot 50:79–88
Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640
Madsen EB, Antolin-Llovera M, Grossmann C, Ye JY, Vieweg S, Broghammer A, Krusell L, Radutoiu S, Jensen ON, Stougaard J, Parniske M (2011) Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J 65:404–417
Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Becard G, Denarie J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63
Matsuzawa SI, Reed JC (2001) Siah-1, SIP, and Ebi collaborate in a novel pathway for β-catenin degradation linked to p53 responses. Mol Cell 7:915–926
Messinese E, Mun JH, Yeun LH, Jayaraman D, Rouge P, Barre A, Lougnon G, Schornack S, Bono JJ, Cook DR, Ane JM (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20:912–921
Miransari M (2011) Interactions between arbuscular mycorrhizal fungi and soil bacteria. Appl Microbiol Biotechnol 89:917–930
Murray JD, Muni RR, Torres-Jerez I, Tang Y, Allen S, Andriankaja M, Li G, Laxmi A, Cheng X, Wen J, Vaughan D, Schultze M, Sun J, Charpentier M, Oldroyd G, Tadege M, Ratet P, Mysore KS, Chen R, Udvardi MK (2011) Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula. Plant J 65:244–252
Nishimura R, Ohmori M, Kawaguchi M (2002) The novel symbiotic phenotype of enhanced-nodulating mutant of Lotus japonicus: astray mutant is an early nodulating mutant with wider nodulation zone. Plant Cell Physiol 43:853–859
Nixon JC, Rajaiya J, Webb CF (2004) Mutations in the DNA-binding domain of the transcription factor Bright act as dominant negative proteins and interfere with immunoglobulin transactivation. J Biol Chem 279:52465–52472
Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546
Oldroyd GE, Long SR (2003) Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod actor signaling. Plant Physiol 131:1027–1032
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775
Pumplin N, Mondo SJ, Topp S, Starker CG, Gantt JS, Harrison MJ (2010) Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J 61:482–494
Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592
Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM, Albrektsen AS, James EK, Thirup S, Stougaard J (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26:3923–3935
Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19:610–624
Sanchez-Lopez R, Jauregui D, Nava N, Alvarado-Affantranger X, Montiel J, Santana O, Sanchez F, Quinto C (2011) Down-regulation of SymRK correlates with a deficiency in vascular bundle development in Phaseolus vulgaris nodules. Plant, Cell Environ 34:2109–2121
Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195
Scott DB, Ronson CW (1982) Identification and mobilization by cointegrate formation of a nodulation plasmid in Rhizobium trifolii. J Bacteriol 151:36–43
Smit P, Raedts J, Portyanko V, Debelle F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789–1791
Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962
Studer S, Narberhaus F (2000) Chaperone activity and homo- and hetero-oligomer formation of bacterial small heat shock proteins. J Biol Chem 275:37212–37218
Tardif M, Brouchon L, Rabiet MJ, Boulay F (2003) Direct binding of a fragment of the Wiskott-Aldrich syndrome protein to the C-terminal end of the anaphylatoxin C5a receptor. Biochem J 372:453–463
Tirichine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen LH, Miwa H, Nakagawa T, Sandal N, Albrektsen AS, Kawaguchi M, Downie A, Sato S, Tabata S, Kouchi H, Parniske M, Kawasaki S, Stougaard J (2006) Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441:1153–1156
Wais RJ, Keating DH, Long SR (2002) Structure-function analysis of nod factor-induced root hair calcium spiking in Rhizobium-legume symbiosis. Plant Physiol 129:211–224
Wilsker D, Patsialou A, Dallas PB, Moran E (2002) ARID proteins: a diverse family of DNA binding proteins implicated in the control of cell growth, differentiation, and development. Cell Growth Differ 13:95–106
Yano K, Yoshida S, Muller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci USA 105:20540–20545
Zhu H, Chen T, Zhu M, Fang Q, Kang H, Hong Z, Zhang Z (2008) A novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus. Plant Physiol 148:337–347
Acknowledgments
This work was supported by the National Basic Research Program of China (973 Program grant no. 2010CB126502), the National Natural Science Foundation of China (grant no. 31170224, 30900096), the Ministry of Agriculture of China (grant no. 2009ZX08009-116B), the Fok Ying-Tong Education Foundation, China (grant no. 122038), the Fundamental Research Funds for the Central Universities (grant no. 2011PY136), the Huazhong Agricultural University Scientific & Technological Self-innovation Foundation (grant no.2011SC02) and the China National Fundamental Fund of Personnel Training (Grant no. J1103510).
Author information
Authors and Affiliations
Corresponding author
Additional information
Chao Wang and Hui Zhu contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, C., Zhu, H., Jin, L. et al. Splice variants of the SIP1 transcripts play a role in nodule organogenesis in Lotus japonicus . Plant Mol Biol 82, 97–111 (2013). https://doi.org/10.1007/s11103-013-0042-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-013-0042-3