Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis.
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.
Zhang
Quan
Q
Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York 14853, USA.
Blaylock
Laura A
LA
Harrison
Maria J
MJ
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
D018528:ATP-Binding Cassette Transporters; D010940:Plant Proteins
Science. 2004 Feb 27;303(5662):1364-7
14963334
Annu Rev Plant Biol. 2007;58:347-75
17263663
Trends Plant Sci. 2008 Apr;13(4):151-9
18299247
Nature. 2006 Jun 29;441(7097):1153-6
16810257
Science. 2007 Oct 12;318(5848):265-8
17932296
Plant J. 2006 Jul;47(2):165-73
16762030
DNA Res. 2006 Oct 31;13(5):205-28
17164256
Plant Cell. 2005 Dec;17(12):3489-99
16284314
Mol Cell. 2002 Apr;9(4):789-98
11983170
Plant Physiol. 2003 Mar;131(3):952-62
12644648
Int Rev Cell Mol Biol. 2009;276:263-99
19584015
Cancer Res. 1998 Dec 1;58(23):5337-9
9850061
New Phytol. 1990 Jul;115(3):495-501
33874272
Plant Physiol. 2007 Jun;144(2):673-81
17142489
FEBS Lett. 2006 Feb 13;580(4):1010-6
16413546
Nature. 2002 Jun 27;417(6892):959-62
12087405
Nature. 2008 Sep 11;455(7210):195-200
18690207
Plant J. 2010 Feb 1;61(3):482-94
19912567
Plant Cell. 2001 May;13(5):1095-107
11340184
Am J Bot. 2007 Nov;94(11):1756-77
21636371
Nature. 2005 Jun 9;435(7043):824-7
15944706
Plant Cell. 2008 May;20(5):1407-20
18515499
FEBS Lett. 2006 Feb 13;580(4):1123-30
16506311
Nature. 2005 Feb 3;433(7025):527-31
15616514
Proc Natl Acad Sci U S A. 2005 May 3;102(18):6285-90
15845768
Plant Physiol. 2009 Oct;151(2):809-19
19692536
Plant Cell. 2008 Nov;20(11):2989-3005
19033527
BMC Plant Biol. 2009 Jan 22;9:10
19161626
Phytochemistry. 2007 Jan;68(1):8-18
17081575
J Lipid Res. 2001 Oct;42(10):1513-20
11590207
Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11841-3
11607500
Plant J. 2007 Sep;51(5):739-50
17573800
Nat Biotechnol. 2005 Sep;23(9):1177-80
16116418
Plant J. 2007 May;50(3):529-44
17419842
Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1720-5
17242358
Nat Rev Mol Cell Biol. 2009 Mar;10(3):218-27
19234479
Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):13324-9
12271140
Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20540-5
19074278
Plant Cell. 2007 Feb;19(2):610-24
17307929
Plant Cell. 2003 Sep;15(9):2106-23
12953114
J Clin Invest. 2002 Sep;110(5):605-9
12208859
Annu Rev Cell Biol. 1992;8:67-113
1282354
Plant J. 2009 Jun;58(5):766-77
19220794
Plant J. 2007 Nov;52(3):485-98
17727615
Nat Rev Microbiol. 2008 Oct;6(10):763-75
18794914
Plant Cell. 2002 Oct;14(10):2413-29
12368495
Mol Plant Microbe Interact. 2001 Jun;14(6):695-700
11386364
Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9823-8
18606999
Plant Physiol. 2008 Sep;148(1):402-13
18614712
J Clin Invest. 2002 Sep;110(5):659-69
12208867
Pflugers Arch. 2007 Feb;453(5):735-44
16983557
EMBO J. 2008 Oct 22;27(20):2648-55
18818697
Science. 2006 Sep 15;313(5793):1596-604
16973872
Plant Cell. 2006 Mar;18(3):731-46
16473969
Plant J. 2002 Jun;30(6):649-62
12061897
Nature. 2002 Jun 27;417(6892):962-6
12087406
Mol Plant Microbe Interact. 2007 Aug;20(8):912-21
17722695
Nature. 2008 Sep 11;455(7210):189-94
18690209
Funct Plant Biol. 2002 Oct;29(10):1217-1225
32689574
Plant Cell Physiol. 2006 Jul;47(7):807-17
16774930
New Phytol. 2004 Sep;163(3):661-668
33873748
Mycorrhiza. 2006 Jul;16(5):299-363
16845554
PLoS Biol. 2006 Jul;4(7):e226
16787107
Proc Natl Acad Sci U S A. 2006 Jan 10;103(2):359-64
16407163
Planta. 2002 Jan;214(3):345-55
11855639
New Phytol. 1988 Feb;108(2):211-218
33874168
New Phytol. 2008;178(4):695-698
18476912
Comput Appl Biosci. 1996 Aug;12(4):357-8
8902363
Science. 2004 Oct 22;306(5696):702-4
15499022