title: The physiological basis for genetic variation in water use efficiency and carbon isotope composition in Arabidopsis thaliana.
abstract: Ecologists and physiologists have documented extensive variation in water use efficiency (WUE) in Arabidopsis thaliana, as well as association of WUE with climatic variation. Here, we demonstrate correlations of whole-plant transpiration efficiency and carbon isotope composition (δ(13)C) among life history classes of A. thaliana. We also use a whole-plant cuvette to examine patterns of co-variation in component traits of WUE and δ(13)C. We find that stomatal conductance (g s) explains more variation in WUE than does A. Overall, there was a strong genetic correlation between A and g s, consistent with selection acting on the ratio of these traits. At a more detailed level, genetic variation in A was due to underlying variation in both maximal rate of carboxylation (V cmax) and maximum electron transport rate (Jmax). We also found strong effects of leaf anatomy, where lines with lower WUE had higher leaf water content (LWC) and specific leaf area (SLA), suggesting a role for mesophyll conductance (g m) in variation of WUE. We hypothesize that this is due to an effect through g m, and test this hypothesis using the abi4 mutant. We show that mutants of ABI4 have higher SLA, LWC, and g m than wild-type, consistent with variation in leaf anatomy causing variation in g m and δ(13)C. These functional data also add further support to the central, integrative role of ABI4 in simultaneously altering ABA sensitivity, sugar signaling, and CO2 assimilation. Together our results highlight the need for a more holistic approach in functional studies, both for more accurate annotation of gene function and to understand co-limitations to plant growth and productivity.
authors.affiliation: Department of Land, Air & Water Resources, University of California, Davis, CA, 95616, USA, heaslon@ucdavis.edu.
authors.forename: Hsien Ming
authors.initials: HM
authors.lastname: Easlon
authors.forename: Krishna S
authors.initials: KS
authors.lastname: Nemali
authors.forename: James H
authors.initials: JH
authors.lastname: Richards
authors.forename: David T
authors.initials: DT
authors.lastname: Hanson
authors.forename: Thomas E
authors.initials: TE
authors.lastname: Juenger
authors.forename: John K
authors.initials: JK
authors.lastname: McKay
mesh_terms: D000040:Abscisic Acid / Q000494:pharmacology; D017360:Arabidopsis / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics; D002245:Carbon Dioxide / Q000378:metabolism; D002247:Carbon Isotopes / Q000378:metabolism*; D004579:Electron Transport / Q000235:genetics; D014644:Genetic Variation; D058503:Mesophyll Cells / Q000502:physiology; D009154:Mutation; D018515:Plant Leaves / Q000033:anatomy & histology / Q000378:metabolism; D054046:Plant Stomata / Q000502:physiology; D018526:Plant Transpiration / Q000235:genetics / Q000502:physiology; D014157:Transcription Factors / Q000235:genetics; D014867:Water / Q000378:metabolism*
chemical_list: C470421:ABI4 protein, Arabidopsis; D029681:Arabidopsis Proteins; D002247:Carbon Isotopes; D014157:Transcription Factors; D014867:Water; D002245:Carbon Dioxide; D000040:Abscisic Acid
references.citation: Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13730-4
references.pmid: 9391094
references.citation: Plant Cell Environ. 2013 Mar;36(3):542-52
references.pmid: 22897236
references.citation: Plant Physiol. 2006 Feb;140(2):411-32
references.pmid: 16407444
references.citation: J Exp Bot. 2002 Feb;53(367):195-200
references.pmid: 11807122
references.citation: Planta. 2011 Sep;234(3):555-63
references.pmid: 21553123
references.citation: Plant Cell. 2008 Mar;20(3):648-57
references.pmid: 18349152
references.citation: Mol Ecol. 2003 May;12(5):1137-51
references.pmid: 12694278
references.citation: Trends Ecol Evol. 2011 Feb;26(2):88-95
references.pmid: 21196061
references.citation: Photosynth Res. 2012 Sep;113(1-3):207-19
references.pmid: 22791015
references.citation: Plant Cell Environ. 2010 Jul;33(7):1176-85
references.pmid: 20199618
references.citation: Plant J. 2008 Aug;55(3):372-81
references.pmid: 18410483
references.citation: Plant Signal Behav. 2011 May;6(5):694-6
references.pmid: 21448003
references.citation: Plant Cell Environ. 2008 May;31(5):602-21
references.pmid: 17996013
references.citation: Plant J. 1997 Nov;12(5):1011-20
references.pmid: 9418043
references.citation: PLoS One. 2008 Feb 27;3(2):e1705
references.pmid: 18301780
references.citation: Plant Cell Environ. 2007 Oct;30(10):1284-98
references.pmid: 17727418
references.citation: Plant Cell Environ. 2012 May;35(5):839-56
references.pmid: 22070625
references.citation: Oecologia. 1997 Feb;109(4):535-546
references.pmid: 28307337
references.citation: Plant Cell Environ. 2006 Feb;29(2):192-201
references.pmid: 17080635
references.citation: Plant Cell Environ. 2007 Sep;30(9):1035-40
references.pmid: 17661745
references.citation: J Exp Bot. 2009;60(8):2235-48
references.pmid: 19395390
references.citation: Tree Physiol. 2008 Jan;28(1):11-9
references.pmid: 17938109
references.citation: Plant J. 2011 Sep;67(5):795-804
references.pmid: 21564354
references.citation: Plant Physiol. 2000 Dec;124(4):1752-65
references.pmid: 11115891
references.citation: Nature. 2005 Aug 11;436(7052):866-70
references.pmid: 16007076
references.citation: Plant Cell. 1998 Jun;10(6):1043-54
references.pmid: 9634591
references.citation: Ann Bot. 2002 Jun;89 Spec No:925-40
references.pmid: 12102518
references.citation: Plant Cell. 2012 Mar;24(3):893-914
references.pmid: 22408074
references.citation: Plant Cell Environ. 2008 Aug;31(8):1170-8
references.pmid: 18510710
references.citation: Plant Physiol. 2011 Jan;155(1):108-16
references.pmid: 21075960
references.citation: Evolution. 2008 Dec;62(12):3014-26
references.pmid: 18691264
references.citation: Plant J. 2009 Aug;59(3):359-74
references.pmid: 19392689
references.citation: Evolution. 2005 Apr;59(4):826-37
references.pmid: 15926692
references.citation: Ann Bot. 2010 Mar;105(3):431-42
references.pmid: 19995810
references.citation: Plant Physiol. 1990 Nov;94(3):1024-32
references.pmid: 16667792
references.citation: Mol Ecol. 2012 Nov;21(22):5512-29
references.pmid: 22857709
references.citation: Plant Cell Environ. 2010 Aug 1;33(8):1268-84
references.pmid: 20302603
references.citation: Plant J. 2000 Sep;23(5):577-85
references.pmid: 10972884
references.citation: Crop Sci. 2002 Jan;42(1):122-131
references.pmid: 11756262
references.citation: Plant J. 2001 Dec;28(6):655-62
references.pmid: 11851911
references.citation: PLoS Biol. 2005 Jul;3(7):e196
references.pmid: 15907155
references.citation: Plant Cell. 2011 Sep;23(9):3319-34
references.pmid: 21926335
references.citation: J Exp Bot. 2012 Feb;63(4):1637-61
references.pmid: 22371324
references.citation: Oecologia. 2008 Mar;155(3):441-54
references.pmid: 18224341
references.citation: Planta. 1980 Jun;149(1):78-90
references.pmid: 24306196
references.citation: Sci Rep. 2012;2:538
references.pmid: 22844579
references.citation: Plant Physiol. 2011 May;156(1):90-105
references.pmid: 21441385
references.citation: Plant Cell Environ. 2007 Apr;30(4):469-82
references.pmid: 17324233