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.
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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
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
Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotechnol 20:642–650
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
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
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
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
Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary developmental perspective. Trends Plant Sci 13:492–498
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
Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304
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
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
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
Chen F, Bradford KJ (2000) Expression of an expansin is associated with endosperm weakening during tomato seed germination. Plant Physiol 124:1265–1274
Cho HT, Cosgrove DJ (2002) Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell 14:3237–3253
Cosgrove DJ (2000a) New genes and new biological roles for expansins. Curr Opin Plant Biol 3:73–78
Cosgrove DJ (2000b) Loosening of plant cell walls by expansins. Nature 407:321–326
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
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
Deising HB, Werner S, Wernitz M (2000) The role of fungal appressoria in plant infection. Microbes Infect 2:1631–1641
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
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
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
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
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
Georgelis N, Nikolaidis N, Cosgrove DJ (2015) Bacterial expansins and related proteins from the world of microbes. Appl Microbiol Biotechnol 99:3807–3823
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
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
Lee Y, Kende H (2001) Expression of beta-expansins is correlated with Internodal elongation in deepwater rice. Plant Physiol 127:645–654
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
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
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
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
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
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
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
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
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
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
McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433
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
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
Oldroyd GED, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5:566–576
Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546
Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 3:320–328
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775
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
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
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
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
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
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
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
Spaink HP (1995) The molecular basis of infection and nodulation by rhizobia: the ins and outs of sympathogenesis. Annu Rev Phytopathol 33:345–368
Sprent JI (2008) 60Ma of legume nodulation. What’s new? What’s changing? J Exp Bot 59:1081–1084
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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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.
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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
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DOI: https://doi.org/10.1007/s13199-017-0501-8