title: Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis.
abstract: In the symbiotic association of plants and arbuscular mycorrhizal (AM) fungi, the fungal symbiont resides in the root cortical cells where it delivers mineral nutrients to its plant host through branched hyphae called arbuscules. Here, we report a Medicago truncatula mutant, stunted arbuscule (str), in which arbuscule development is impaired and AM symbiosis fails. In contrast with legume symbiosis mutants reported previously, str shows a wild-type nodulation phenotype. STR was identified by positional cloning and encodes a half-size ATP binding cassette (ABC) transporter of a subfamily (ABCG) whose roles in plants are largely unknown. STR is a representative of a novel clade in the ABCG subfamily, and its orthologs are highly conserved throughout the vascular plants but absent from Arabidopsis thaliana. The STR clade is unusual in that it lacks the taxon-specific diversification that is typical of the ABCG gene family. This distinct phylogenetic profile enabled the identification of a second AM symbiosis-induced half-transporter, STR2. Silencing of STR2 by RNA interference results in a stunted arbuscule phenotype identical to that of str. STR and STR2 are coexpressed constitutively in the vascular tissue, and expression is induced in cortical cells containing arbuscules. STR heterodimerizes with STR2, and the resulting transporter is located in the peri-arbuscular membrane where its activity is required for arbuscule development and consequently a functional AM symbiosis.
authors.affiliation: Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York 14853, USA.
authors.forename: Quan
authors.initials: Q
authors.lastname: Zhang
authors.forename: Laura A
authors.initials: LA
authors.lastname: Blaylock
authors.forename: Maria J
authors.initials: MJ
authors.lastname: Harrison
mesh_terms: D018528:ATP-Binding Cassette Transporters / Q000378:metabolism*; D002462:Cell Membrane / Q000378:metabolism; D003001:Cloning, Molecular; D017124:Conserved Sequence / Q000235:genetics; D018506:Gene Expression Regulation, Plant; D055785:Gene Knockdown Techniques; D025301:Hyphae / Q000166:cytology / Q000254:growth & development*; D046913:Medicago truncatula / Q000166:cytology / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology*; D008969:Molecular Sequence Data; D009154:Mutation / Q000235:genetics; D038821:Mycorrhizae / Q000166:cytology / Q000254:growth & development* / Q000378:metabolism; D010641:Phenotype; D010802:Phylogeny; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D055170:Plant Root Nodulation; D030821:Plants, Genetically Modified; D011485:Protein Binding; D034622:RNA Interference; D013559:Symbiosis
chemical_list: D018528:ATP-Binding Cassette Transporters; D010940:Plant Proteins
references.citation: Science. 2004 Feb 27;303(5662):1364-7
references.pmid: 14963334
references.citation: Annu Rev Plant Biol. 2007;58:347-75
references.pmid: 17263663
references.citation: Trends Plant Sci. 2008 Apr;13(4):151-9
references.pmid: 18299247
references.citation: Nature. 2006 Jun 29;441(7097):1153-6
references.pmid: 16810257
references.citation: Science. 2007 Oct 12;318(5848):265-8
references.pmid: 17932296
references.citation: Plant J. 2006 Jul;47(2):165-73
references.pmid: 16762030
references.citation: DNA Res. 2006 Oct 31;13(5):205-28
references.pmid: 17164256
references.citation: Plant Cell. 2005 Dec;17(12):3489-99
references.pmid: 16284314
references.citation: Mol Cell. 2002 Apr;9(4):789-98
references.pmid: 11983170
references.citation: Plant Physiol. 2003 Mar;131(3):952-62
references.pmid: 12644648
references.citation: Int Rev Cell Mol Biol. 2009;276:263-99
references.pmid: 19584015
references.citation: Cancer Res. 1998 Dec 1;58(23):5337-9
references.pmid: 9850061
references.citation: New Phytol. 1990 Jul;115(3):495-501
references.pmid: 33874272
references.citation: Plant Physiol. 2007 Jun;144(2):673-81
references.pmid: 17142489
references.citation: FEBS Lett. 2006 Feb 13;580(4):1010-6
references.pmid: 16413546
references.citation: Nature. 2002 Jun 27;417(6892):959-62
references.pmid: 12087405
references.citation: Nature. 2008 Sep 11;455(7210):195-200
references.pmid: 18690207
references.citation: Plant J. 2010 Feb 1;61(3):482-94
references.pmid: 19912567
references.citation: Plant Cell. 2001 May;13(5):1095-107
references.pmid: 11340184
references.citation: Am J Bot. 2007 Nov;94(11):1756-77
references.pmid: 21636371
references.citation: Nature. 2005 Jun 9;435(7043):824-7
references.pmid: 15944706
references.citation: Plant Cell. 2008 May;20(5):1407-20
references.pmid: 18515499
references.citation: FEBS Lett. 2006 Feb 13;580(4):1123-30
references.pmid: 16506311
references.citation: Nature. 2005 Feb 3;433(7025):527-31
references.pmid: 15616514
references.citation: Proc Natl Acad Sci U S A. 2005 May 3;102(18):6285-90
references.pmid: 15845768
references.citation: Plant Physiol. 2009 Oct;151(2):809-19
references.pmid: 19692536
references.citation: Plant Cell. 2008 Nov;20(11):2989-3005
references.pmid: 19033527
references.citation: BMC Plant Biol. 2009 Jan 22;9:10
references.pmid: 19161626
references.citation: Phytochemistry. 2007 Jan;68(1):8-18
references.pmid: 17081575
references.citation: J Lipid Res. 2001 Oct;42(10):1513-20
references.pmid: 11590207
references.citation: Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11841-3
references.pmid: 11607500
references.citation: Plant J. 2007 Sep;51(5):739-50
references.pmid: 17573800
references.citation: Nat Biotechnol. 2005 Sep;23(9):1177-80
references.pmid: 16116418
references.citation: Plant J. 2007 May;50(3):529-44
references.pmid: 17419842
references.citation: Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1720-5
references.pmid: 17242358
references.citation: Nat Rev Mol Cell Biol. 2009 Mar;10(3):218-27
references.pmid: 19234479
references.citation: Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):13324-9
references.pmid: 12271140
references.citation: Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20540-5
references.pmid: 19074278
references.citation: Plant Cell. 2007 Feb;19(2):610-24
references.pmid: 17307929
references.citation: Plant Cell. 2003 Sep;15(9):2106-23
references.pmid: 12953114
references.citation: J Clin Invest. 2002 Sep;110(5):605-9
references.pmid: 12208859
references.citation: Annu Rev Cell Biol. 1992;8:67-113
references.pmid: 1282354
references.citation: Plant J. 2009 Jun;58(5):766-77
references.pmid: 19220794
references.citation: Plant J. 2007 Nov;52(3):485-98
references.pmid: 17727615
references.citation: Nat Rev Microbiol. 2008 Oct;6(10):763-75
references.pmid: 18794914
references.citation: Plant Cell. 2002 Oct;14(10):2413-29
references.pmid: 12368495
references.citation: Mol Plant Microbe Interact. 2001 Jun;14(6):695-700
references.pmid: 11386364
references.citation: Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9823-8
references.pmid: 18606999
references.citation: Plant Physiol. 2008 Sep;148(1):402-13
references.pmid: 18614712
references.citation: J Clin Invest. 2002 Sep;110(5):659-69
references.pmid: 12208867
references.citation: Pflugers Arch. 2007 Feb;453(5):735-44
references.pmid: 16983557
references.citation: EMBO J. 2008 Oct 22;27(20):2648-55
references.pmid: 18818697
references.citation: Science. 2006 Sep 15;313(5793):1596-604
references.pmid: 16973872
references.citation: Plant Cell. 2006 Mar;18(3):731-46
references.pmid: 16473969
references.citation: Plant J. 2002 Jun;30(6):649-62
references.pmid: 12061897
references.citation: Nature. 2002 Jun 27;417(6892):962-6
references.pmid: 12087406
references.citation: Mol Plant Microbe Interact. 2007 Aug;20(8):912-21
references.pmid: 17722695
references.citation: Nature. 2008 Sep 11;455(7210):189-94
references.pmid: 18690209
references.citation: Funct Plant Biol. 2002 Oct;29(10):1217-1225
references.pmid: 32689574
references.citation: Plant Cell Physiol. 2006 Jul;47(7):807-17
references.pmid: 16774930
references.citation: New Phytol. 2004 Sep;163(3):661-668
references.pmid: 33873748
references.citation: Mycorrhiza. 2006 Jul;16(5):299-363
references.pmid: 16845554
references.citation: PLoS Biol. 2006 Jul;4(7):e226
references.pmid: 16787107
references.citation: Proc Natl Acad Sci U S A. 2006 Jan 10;103(2):359-64
references.pmid: 16407163
references.citation: Planta. 2002 Jan;214(3):345-55
references.pmid: 11855639
references.citation: New Phytol. 1988 Feb;108(2):211-218
references.pmid: 33874168
references.citation: New Phytol. 2008;178(4):695-698
references.pmid: 18476912
references.citation: Comput Appl Biosci. 1996 Aug;12(4):357-8
references.pmid: 8902363
references.citation: Science. 2004 Oct 22;306(5696):702-4
references.pmid: 15499022