Skip to main content
Log in

Plant-symbiont interactions: the functional role of expansins

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Expansins are non-enzymatic cell wall proteins that mediate plant growth by catalyzing loosening of cell walls without lysing the wall polymers. Advances in the field of bioinformatics have facilitated the prediction of the members of expansin gene family across several model plants. Expansins constitutes into four sub-families; α-expansin, β-expansin, expansin-like A and expansin-like B. Biological functions of expansin gene family include diverse aspects of plant growth and development, shoot and root elongation, leaf morphogenesis, flower and fruit development, embryogenesis, pollen tube growth, stress tolerance, etc. Recent studies have demonstrated the role of expansins in plant-symbiotic interactions. The present review reveals the factors that govern plant-arbuscular mycorrhizal fungi (AMF) and legume-rhizobia symbioses; and the genes that participate in these diverse symbiont interactions. Further, we focus on the expression profiles and the functions of expansins during plant-AMF and legume-rhizobia interactions. The key roles of expansin proteins during AMF invasion, arbuscule formation, rhizobial infection and nodule organogenesis were uncovered during symbioses. This review summarizes discoveries that support the key and versatile roles of various expansin members in the plant-mycorrhizal and legume-rhizobial symbioses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Lévy J, Debellé F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367

    Article  PubMed  Google Scholar 

  • Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, Mirabella R, de Carvalho-Niebel F, Journet EP, Ghérardi M, Huguet T, Geurts R, Dénarié J, Rougé P, Gough C (2006) The Medicago truncatula lysin motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142:265–279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotechnol 20:642–650

    Article  CAS  PubMed  Google Scholar 

  • Balestrini R, Cosgrove DJ, Bonfante P (2005) Differential location of α-expansin proteins during the accommodation of root cells to an arbuscular mycorrhizal fungus. Planta 220:889–899

    Article  CAS  PubMed  Google Scholar 

  • Balestrini R, Ott T, Güther M, Bonfante P, Udvardi MK, De Tullio MC (2012) Ascorbate oxidase: the unexpected involvement of a 'wasteful enzyme' in the symbioses with nitrogen-fixing bacteria and arbuscular mycorrhizal fungi. Plant Physiol Biochem 59:71–79

    Article  CAS  PubMed  Google Scholar 

  • Belfield EJ, Ruperti B, Roberts JA, McQueen-Mason S (2005) Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission in Sambucus nigra. J Exp Bot 56:817–823

    Article  CAS  PubMed  Google Scholar 

  • Besserer A, Puech-Pagés V, Kiefer P, Gómez-Roldán V, Jauneau A, Roy S et al (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:e226

    Article  PubMed  PubMed Central  Google Scholar 

  • Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary developmental perspective. Trends Plant Sci 13:492–498

    Article  CAS  PubMed  Google Scholar 

  • Boron AK, Van Loock B, Suslov D, Markakis MN, Verbelen JP, Vissenberg K (2015) Over-expression of AtEXLA2 alters etiolated Arabidopsis hypocotyl growth. Ann Bot 115:67–80

    Article  CAS  PubMed  Google Scholar 

  • Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304

    Article  Google Scholar 

  • van Brussel AAN, Bakhuizen R, Vanspronsen PC, Spaink HP, Tak T, Lugtenberg BJJ et al (1992) Induction of preinfection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium. Science 257:70–72

    Article  PubMed  Google Scholar 

  • de Carvalho GAB, Batista JSS, Marcelino-Guimarães FC, do Nascimento LC, Hungria M (2013) Transcriptional analysis of genes involved in nodulation in soybean roots inoculated with Bradyrhizobium japonicum strain CPAC 15. BMC Genomics 14:153

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen F, Bradford KJ (2000) Expression of an expansin is associated with endosperm weakening during tomato seed germination. Plant Physiol 124:1265–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho HT, Cosgrove DJ (2002) Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell 14:3237–3253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove DJ (2000a) New genes and new biological roles for expansins. Curr Opin Plant Biol 3:73–78

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2000b) Loosening of plant cell walls by expansins. Nature 407:321–326

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ, Bedinger P, Durachko DM (1997) Group I allergens of grass pollen as cell wall-loosening agents. Proc Natl Acad Sci U S A 94:6559–6564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove DJ, Li LC, Cho HT, Hoffmann-Benning S, Moore RC, Blecker D (2002) The growing world of expansins. Plant Cell Physiol 43:1436–1444

    Article  CAS  PubMed  Google Scholar 

  • Deising HB, Werner S, Wernitz M (2000) The role of fungal appressoria in plant infection. Microbes Infect 2:1631–1641

    Article  CAS  PubMed  Google Scholar 

  • Dermatsev V, Weingarten-baror C, Resnick N, Gadkar V, Wininger S, Kolotilin I, Mayzlish-gati E, Zilberstein A, Koltai H, Kapulnik Y (2010) Microarray analysis and functional tests suggest the involvement of expansins in the early stages of symbiosis of the arbuscular mycorrhizal fungus Glomus intraradices on tomato (Solanum lycopersicum). Mol Plant Pathol 11:121–135

    Article  CAS  PubMed  Google Scholar 

  • Devi MJ, Taliercio EW, Sinclair TR (2015) Leaf expansion of soybean subjected to high and low atmospheric vapour pressure deficits. J Exp Bot 66:1845–1850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flemetakis E, Efrose RC, Desbrosses G, Dimou M, Delis C, Aivalakis G, Udvardi MK, Katinakis P (2004) Induction and spatial organization of polyamine biosynthesis during nodule development in Lotus japonicus. Mol Plant-Microbe Interact 17:1283–1293

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genre A, Chabaud M, Balzergue C, Puech-Pages V, Novero M, Rey T, Fournier J, Rochange S, Becard G, Bonfante P et al (2013) Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 198:190–202

    Article  PubMed  Google Scholar 

  • Georgelis N, Nikolaidis N, Cosgrove DJ (2015) Bacterial expansins and related proteins from the world of microbes. Appl Microbiol Biotechnol 99:3807–3823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret 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 Frankiabacteria. Proc Natl Acad Sci U S A 105:4928–4932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giordano W, Hirsch AM (2004) The expression of MaEXP1, a Melilotus alba expansin gene, is upregulated during the sweetclover-Sinorhizobium meliloti inter action. Mol Plant-Microbe Interact 17:613–622

    Article  CAS  PubMed  Google Scholar 

  • Godfroy O, Debelle F, Timmer T, Rosenberg C (2006) A rice calcium-and calmodulin-dependent kinase restores nodulation to a legume mutant. Mol Plant-Microbe Interact 19:495–501

    Article  CAS  PubMed  Google Scholar 

  • Gray-Mitsumune M, Mellerowicz EJ, Abe H, Schrader J, Winzéll A, Sterky F, Blomqvist K, McQueen-Mason S, Teeri TT, Sundberg B (2004) Expansins abundant in secondary xylem belong to subgroup A of the α-expansin gene family. Plant Physiol 135:1552–1564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groth M, Takeda N, Perry J, Uchida H, Dräxl S, Brachmann A et al (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P (2009) Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 182:200–212

    Article  CAS  PubMed  Google Scholar 

  • Guo W, Zhao J, Li X, Qin L, Yan X, Liao H (2011) A soybean ß-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant J 66:541–552

    Article  CAS  PubMed  Google Scholar 

  • Györgyey J, Vaubert D, Jiménez-Zurdo JI, Charon C, Troussard L, Kondorosi A, Kondorosi E (2000) Analysis of Medicago truncatula nodule expressed sequence tags. Mol Plant-Microbe Interact 13:62–71

    Article  PubMed  Google Scholar 

  • Han Y, Chen Y, Yin S, Zhang M, Wang W (2015) Over-expression of TaEXPB23, a wheat expansin gene, improves oxidative stress tolerance in transgenic tobacco plants. J Plant Physiol 173:62–71

    Article  CAS  PubMed  Google Scholar 

  • Hayashi T, Banba M, Shimoda Y, Kouchi H, Hayashi M, Imaizumi-Anraku H (2010) A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J 63:141–154

    CAS  PubMed  PubMed Central  Google Scholar 

  • He X, Zeng J, Cao F, Ahmed IM, Zhang G, Vincze E, Wu F (2015) HvEXPB7, a novel β-expansin gene revealed by the root hair transcriptome of Tibetan wild barley, improves root hair growth under drought stress. J Exp Bot 66:7405–7419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EMH, 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 U S A 103:359–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kende H, Bradford K, Brummell D, Cho HT, Cosgrove DJ, Fleming AJ, Gehring C, Lee Y, McQueen-Mason S, Rose J, Voesenek L (2004) Nomenclature for members of the expansin superfamily of genes and proteins. Plant Mol Biol 55:311–314

    Article  CAS  PubMed  Google Scholar 

  • Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb KJ, Szczyglowski K, Parniske M (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17:2217–2229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Kwasniewski M, Szarejko I (2006) Molecular cloning and characterization of beta-expansin gene related to root hair formation in barley. Plant Physiol 141:1149–1158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee Y, Kende H (2001) Expression of beta-expansins is correlated with Internodal elongation in deepwater rice. Plant Physiol 127:645–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee HW, Kim J (2013) EXPANSINA17 up-regulated by LBD18/ASL20 promotes lateral root formation during the auxin response. Plant Cell Physiol 54:1600–1611

    Article  CAS  PubMed  Google Scholar 

  • Lee DK, Ahn JH, Song S-K, Choi YD, Lee JS (2003) Expression of an expansin gene is correlated with root elongation in soybean. Plant Physiol 131:985–997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané JM, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364

    Article  PubMed  Google Scholar 

  • Li X, Zhao J, Walk TC, Liao H (2014) Characterization of soybean β-expansin genes and their expression responses to symbiosis, nutrient deficiency, and hormone treatment. Appl Microbiol Biotechnol 98:2805–2817

    Article  CAS  PubMed  Google Scholar 

  • Li X, Zhao J, Tan Z, Zeng R, Liao H (2015) GmEXPB2, a cell wall ß-expansin, affects soybean nodulation through modifying root architecture and promoting nodule formation and development. Plant Physiol 169:2640–2653

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lü P, Kang M, Jiang X, Dai F, Gao J, Zhang C (2013) RhEXPA4, a rose expansin gene, modulates leaf growth and confers drought and salt tolerance to Arabidopsis. Planta 237:1547–1559

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63

    Article  CAS  PubMed  Google Scholar 

  • McQueen-Mason S, Cosgrove DJ (1994) Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci U S A 1:6574–6578

    Article  Google Scholar 

  • McQueen-Mason SJ, Cosgrove DJ (1995) Expansin mode of action on cell walls. Analysis of wall hydrolysis, stress relaxation, and binding. Plant Physiol 107:87–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyahara A, Richens J, Starker C, Morieri G, Smith L, Long S, Downie JA, Oldroyd GED (2010) Conservation in function of a SCAR/WAVE component during infection thread and root hair growth in Medicago truncatula. Mol Plant Microbe Interact 23:1553–1562

    Article  CAS  PubMed  Google Scholar 

  • Nardi CF, Villarreal NM, Rossi FR, Martínez S, Martínez GA, Civello PM (2015) Overexpression of the carbohydrate binding module of strawberry expansin2 in Arabidopsis thaliana modifies plant growth and cell wall metabolism. Plant Mol Biol 88:101–117

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GED, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5:566–576

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546

    Article  CAS  PubMed  Google Scholar 

  • Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 3:320–328

    Article  CAS  PubMed  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775

    Article  CAS  PubMed  Google Scholar 

  • Pezzotti M, Feron R, Mariani C (2002) Pollination modulates expression of the PPAL gene, a pistil-specific beta-expansin. Plant Mol Biol 49:187–197

    Article  CAS  PubMed  Google Scholar 

  • Robledo M, Jiménez-Zurdo JI, Velázquez E, Trujillo ME, Zurdo-Piñeiro JL, Ramírez-Bahena MH, Ramos B, Díaz-Mínguez JM, Dazzo F, Martínez-Molina E, Mateos PF (2008) Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots. Proc Natl Acad Sci U S A 105:7064–7069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasidharan R, Chinnappa CC, Staal M, Elzenga JTM, Yokoyama R, Nishitani K et al (2010) Light quality-mediated petiole elongation in Arabidopsis during shade avoidance involves Cell Wall modification by xyloglucan Endotransglucosylase/hydrolases. Plant Physiol 154:978–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaller A, Stintzi A, Graff L (2012) Subtilases - versatile tools for protein turnover, plant development, and interactions with the environment. Physiol Plant 145:52–66

    Article  CAS  PubMed  Google Scholar 

  • Siciliano V, Genre A, Balestrini R, Cappellazzo G, deWit PJGM, Bonfante P (2007) Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 144:1455–1466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Spaink HP (1995) The molecular basis of infection and nodulation by rhizobia: the ins and outs of sympathogenesis. Annu Rev Phytopathol 33:345–368

    Article  CAS  PubMed  Google Scholar 

  • Sprent JI (2008) 60Ma of legume nodulation. What’s new? What’s changing? J Exp Bot 59:1081–1084

    Article  CAS  PubMed  Google Scholar 

  • van Spronsen PC, Bakhuizen R, van Brussel AA, Kijne JW (1994) Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process. Eur J Cell Biol 64:88–94

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sujkowska M, Borucki W, Golinowski W (2007) Localization of expansin-like protein in apoplast of pea (Pisum sativum L.) root nodules during interaction with Rhizobium leguminosarum bv. viciae. Acta Soc Bot Pol 76:17–26

    Article  CAS  Google Scholar 

  • Takeda N, Sato S, Asamizu E, Tabata S, Parniske M (2009) Apoplastic plant subtilases support arbuscular mycorrhiza development in Lotus japonicus. Plant J 58:766–777

    Article  CAS  PubMed  Google Scholar 

  • Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A et al (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769

    Article  CAS  PubMed  Google Scholar 

  • Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R et al (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 110:20117–20122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veneault-Fourrey C, Commun C, Kohler A, Morin E, Balestrini R, Plett J, Danchin E, Coutinho P, Wiebenga A, de Vries RP, Henrissat B, Martin F (2014) Genomic and transcriptomic analysis of Laccaria bicolor CAZome reveals insights into polysaccharides remodelling during symbiosis establishment. Fungal Genet Biol 72:168–181

    Article  CAS  PubMed  Google Scholar 

  • Wei P, Chen S, Zhang X, Zhao P, Xiong Y, Wang W, Wang X (2011) An a-expansin, VfEXPA1, is involved in regulation of stomatal movement in Vicia faba L. Chin Sci Bull 56:3531–3537

    Article  CAS  Google Scholar 

  • Willmann M, Gerlach N, Buer B, Polatajko A, Nagy R, Koebke E, Jansa J, Flisch R, Bucher M (2013) Mycorrhizal phosphate uptake pathway in maize: vital for growth and cob development on nutrient poor agricultural and greenhouse soils. Front Plant Sci 4:533

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiśniewska M, Golinowski W (2011) Immunolocalization of α-expansin protein (ntexpa5) in tobacco roots in the presence of the arbuscular mycorrhizal fungus Glomus mosseae Nicol. & Gerd. Acta biologicacracoviensia Series Botanica 53:113–123

    Google Scholar 

  • Won S-K, Choi S-B, Kumari S, Cho M, Lee SH, Cho H-T (2010) Root hair specific EXPANSIN B genes have been selected for graminaceae root hairs. Mol Cells 30:369–376

    Article  CAS  PubMed  Google Scholar 

  • Xie F, Murray JD, Kim J, Heckmann AB, Edwards A, Oldroyd GED, Downie JA (2012) Legume pectate lyase required for root infection by rhizobia. Proc Natl Acad Sci U S A 109:633–638

    Article  CAS  PubMed  Google Scholar 

  • Yano K, Yoshida S, Müller 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 U S A 105:20540–20545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokota K, Fukai E, Madsen LH, Jurkiewicz A, Rueda P, Radutoiu S et al (2009) Rearrangement of actin cytoskeleton mediates invasion of Lotus japonicus roots by Mesorhizobium loti. Plant Cell 21:267–284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Z, Kang B, He X, Lv S, Bai Y, Ding W, Wu P (2011) Root hair specific expansins modulate root hair elongation in rice. Plant J 66:725–734

    Article  CAS  Google Scholar 

  • Zou H, Wenwen Y, Zang G, Kang Z, Zhang Z, Huang J, Wang G (2015) OsEXPB2, a ß-expansin gene, is involved in rice root system architecture. Mol Breed 35:41

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Consejo Nacional de Ciencia y Tecnològia (CONACYT grant no. 240614), PAPIIT (DGAPA-UNAM grant no. IN219916) to M.L. and DGAPA-UNAM postdoctoral fellowship (DGAP/DG0639/2016) to S.K.M.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Miguel Lara.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mohanty, S.K., Arthikala, MK., Nanjareddy, K. et al. Plant-symbiont interactions: the functional role of expansins. Symbiosis 74, 1–10 (2018). https://doi.org/10.1007/s13199-017-0501-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-017-0501-8

Keywords

Navigation