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Title: A genetic link between leaf carbon isotope composition and whole-plant water use efficiency in the C4 grass Setaria

Abstract

Genetic selection for whole-plant water use efficiency (yield per transpiration; WUEplant) in any crop-breeding programme requires high-throughput phenotyping of component traits of WUEplant such as intrinsic water use efficiency (WUEi; CO2 assimilation rate per stomatal conductance). Measuring WUEi by gas exchange measurements is laborious and time consuming and may not reflect an integrated WUEi over the life of the leaf. Alternatively, leaf carbon stable isotope composition (δ13Cleaf) has been suggested as a potential time-ntegrated proxy for WUEi that may provide a tool to screen for WUEplant. However, a genetic link between δ13Cleaf and WUEplant in a C4 species has not been well established. Thus, to confirm if there is a genetic relationship in a C4 plant between δ13Cleaf and WUEplant under well watered and water-limited growth conditions, a high-throughput phenotyping facility was used to measure WUEplant in a recombinant inbred line (RIL) population created between the C4 grasses Setaria viridis and S. italica . Three quantitative trait loci (QTL) for δ13Cleaf were found and co-localized with transpiration, biomass accumulation, and WUEplant. Additionally, WUEplant for each of the δ13Cleaf QTL allele classes was negatively correlated with δ13Cleaf, as would be predicted when WUEi influences WUEplant. These findings demonstrate that δ13Cleafmore » is genetically linked to WUEplant, likely to be through their relationship with WUEi, and can be used as a high-throughput proxy to screen for WUEplant in these C4 species.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [1]
  1. Washington State Univ., Pullman, WA (United States)
  2. Donald Danforth Plant Science Center, St. Louis, MO (United States)
Publication Date:
Research Org.:
Donald Danforth Plant Science Center, St. Louis, MO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA
OSTI Identifier:
1633319
Alternate Identifier(s):
OSTI ID: 1602562
Grant/Contract Number:  
SC0018277; SC0008769
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 102; Journal Issue: 6; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; quantitative trait loci; leaf carbon isotopes; C4 photosynthesis; Setaria; water use efficiency; phenotyping; genetic architecture; drought; recombinant inbred lines

Citation Formats

Ellsworth, Patrick Z., Feldman, Max J., Baxter, Ivan, and Cousins, Asaph B. A genetic link between leaf carbon isotope composition and whole-plant water use efficiency in the C4 grass Setaria. United States: N. p., 2020. Web. doi:10.1111/tpj.14696.
Ellsworth, Patrick Z., Feldman, Max J., Baxter, Ivan, & Cousins, Asaph B. A genetic link between leaf carbon isotope composition and whole-plant water use efficiency in the C4 grass Setaria. United States. https://doi.org/10.1111/tpj.14696
Ellsworth, Patrick Z., Feldman, Max J., Baxter, Ivan, and Cousins, Asaph B. Wed . "A genetic link between leaf carbon isotope composition and whole-plant water use efficiency in the C4 grass Setaria". United States. https://doi.org/10.1111/tpj.14696. https://www.osti.gov/servlets/purl/1633319.
@article{osti_1633319,
title = {A genetic link between leaf carbon isotope composition and whole-plant water use efficiency in the C4 grass Setaria},
author = {Ellsworth, Patrick Z. and Feldman, Max J. and Baxter, Ivan and Cousins, Asaph B.},
abstractNote = {Genetic selection for whole-plant water use efficiency (yield per transpiration; WUEplant) in any crop-breeding programme requires high-throughput phenotyping of component traits of WUEplant such as intrinsic water use efficiency (WUEi; CO2 assimilation rate per stomatal conductance). Measuring WUEi by gas exchange measurements is laborious and time consuming and may not reflect an integrated WUEi over the life of the leaf. Alternatively, leaf carbon stable isotope composition (δ13Cleaf) has been suggested as a potential time-ntegrated proxy for WUEi that may provide a tool to screen for WUEplant. However, a genetic link between δ13Cleaf and WUEplant in a C4 species has not been well established. Thus, to confirm if there is a genetic relationship in a C4 plant between δ13Cleaf and WUEplant under well watered and water-limited growth conditions, a high-throughput phenotyping facility was used to measure WUEplant in a recombinant inbred line (RIL) population created between the C4 grasses Setaria viridis and S. italica . Three quantitative trait loci (QTL) for δ13Cleaf were found and co-localized with transpiration, biomass accumulation, and WUEplant. Additionally, WUEplant for each of the δ13Cleaf QTL allele classes was negatively correlated with δ13Cleaf, as would be predicted when WUEi influences WUEplant. These findings demonstrate that δ13Cleaf is genetically linked to WUEplant, likely to be through their relationship with WUEi, and can be used as a high-throughput proxy to screen for WUEplant in these C4 species.},
doi = {10.1111/tpj.14696},
journal = {The Plant Journal},
number = 6,
volume = 102,
place = {United States},
year = {Wed Jan 22 00:00:00 EST 2020},
month = {Wed Jan 22 00:00:00 EST 2020}
}

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Works referenced in this record:

Carbon isotope composition, water use efficiency, and drought sensitivity are controlled by a common genomic segment in maize
journal, September 2018

  • Avramova, Viktoriya; Meziane, Adel; Bauer, Eva
  • Theoretical and Applied Genetics, Vol. 132, Issue 1
  • DOI: 10.1007/s00122-018-3193-4

Time dependent genetic analysis links field and controlled environment phenotypes in the model C4 grass Setaria
journal, June 2017


Root traits and δ13C and δ18O of durum wheat under different water regimes
journal, January 2012

  • Elazab, Abdelhalim; Molero, Gemma; Serret, Maria Dolores
  • Functional Plant Biology, Vol. 39, Issue 5
  • DOI: 10.1071/FP11237

The physiological basis for genetic variation in water use efficiency and carbon isotope composition in Arabidopsis thaliana
journal, July 2013

  • Easlon, Hsien Ming; Nemali, Krishna S.; Richards, James H.
  • Photosynthesis Research, Vol. 119, Issue 1-2
  • DOI: 10.1007/s11120-013-9891-5

Improving water use efficiency of vineyards in semi-arid regions. A review
journal, December 2014

  • Medrano, Hipólito; Tomás, Magdalena; Martorell, Sebastiá
  • Agronomy for Sustainable Development, Vol. 35, Issue 2
  • DOI: 10.1007/s13593-014-0280-z

Comparative ecophysiology of leaf and canopy photosynthesis
journal, October 1995


Carbon isotope discrimination as a tool to explore C4 photosynthesis
journal, April 2014

  • Caemmerer, Susanne von; Ghannoum, Oula; Pengelly, Jasper J. L.
  • Journal of Experimental Botany, Vol. 65, Issue 13
  • DOI: 10.1093/jxb/eru127

Predicted versus measured photosynthetic water-use efficiency of crop stands under dynamically changing field environments
journal, September 2004


Shade compromises the photosynthetic efficiency of NADP-ME less than that of PEP-CK and NAD-ME C4 grasses
journal, April 2018

  • Sonawane, Balasaheb V.; Sharwood, Robert E.; Whitney, Spencer
  • Journal of Experimental Botany, Vol. 69, Issue 12
  • DOI: 10.1093/jxb/ery129

Breeding for high water-use efficiency
journal, September 2004

  • Condon, A. G.
  • Journal of Experimental Botany, Vol. 55, Issue 407
  • DOI: 10.1093/jxb/erh277

Net carbon exchange in grapevine canopies responds rapidly to timing and extent of regulated deficit irrigation
journal, January 2011

  • Tarara, Julie M.; Peña, Jorge E. Perez; Keller, Markus
  • Functional Plant Biology, Vol. 38, Issue 5
  • DOI: 10.1071/FP10221

A Versatile Phenotyping System and Analytics Platform Reveals Diverse Temporal Responses to Water Availability in Setaria
journal, October 2015


Stomatal Size, Speed, and Responsiveness Impact on Photosynthesis and Water Use Efficiency
journal, February 2014


Identification of causal relationships among traits related to drought resistance in Stylosanthes scabra using QTL analysis
journal, February 2001

  • Thumma, Bala R.; Naidu, Bodapati P.; Chandra, Amaresh
  • Journal of Experimental Botany, Vol. 52, Issue 355
  • DOI: 10.1093/jxb/52.355.203

Improving Intrinsic Water-Use Efficiency and Crop Yield
journal, January 2002


Foxtail Millet: A Sequence-Driven Grass Model System: Figure 1.
journal, January 2009

  • Doust, Andrew N.; Kellogg, Elizabeth A.; Devos, Katrien M.
  • Plant Physiology, Vol. 149, Issue 1
  • DOI: 10.1104/pp.108.129627

Improving water use in crop production
journal, July 2007

  • Morison, J. I. L.; Baker, N. R.; Mullineaux, P. M.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1491
  • DOI: 10.1098/rstb.2007.2175

Yield improvement and adaptation of wheat to water-limited environments in Australia—a case study
journal, January 2014

  • Richards, R. A.; Hunt, J. R.; Kirkegaard, J. A.
  • Crop and Pasture Science, Vol. 65, Issue 7
  • DOI: 10.1071/CP13426

Carbon Isotope Discrimination is Positively Correlated with Grain Yield and Dry Matter Production in Field-Grown Wheat1
journal, January 1987


From leaf to whole-plant water use efficiency (WUE) in complex canopies: Limitations of leaf WUE as a selection target
journal, June 2015

  • Medrano, Hipólito; Tomás, Magdalena; Martorell, Sebastià
  • The Crop Journal, Vol. 3, Issue 3
  • DOI: 10.1016/j.cj.2015.04.002

Oxygen isotope enrichment (Δ 18 O) reflects yield potential and drought resistance in maize
journal, November 2009


Genome-wide association study (GWAS) of carbon isotope ratio (δ13C) in diverse soybean [Glycine max (L.) Merr.] genotypes
journal, November 2014

  • Dhanapal, Arun Prabhu; Ray, Jeffery D.; Singh, Shardendu K.
  • Theoretical and Applied Genetics, Vol. 128, Issue 1
  • DOI: 10.1007/s00122-014-2413-9

Increasing water use efficiency of irrigated sugarcane production in South Africa through better agronomic practices
journal, May 2015


Combined use of δ13C, δ18O and δ15N tracks nitrogen metabolism and genotypic adaptation of durum wheat to salinity and water deficit
journal, February 2012


Carbon isotopes and water use efficiency in C4 plants
journal, June 2016


Acclimation of C4 metabolism to low light in mature maize leaves could limit energetic losses during progressive shading in a crop canopy
journal, March 2014

  • Bellasio, Chandra; Griffiths, Howard
  • Journal of Experimental Botany, Vol. 65, Issue 13
  • DOI: 10.1093/jxb/eru052

Photosynthetic flexibility in maize exposed to salinity and shade
journal, April 2014

  • Sharwood, R. E.; Sonawane, B. V.; Ghannoum, O.
  • Journal of Experimental Botany, Vol. 65, Issue 13
  • DOI: 10.1093/jxb/eru130

Isotopic analyses based on the mass spectra of carbon dioxide
journal, June 1985

  • Santrock, Jeffrey.; Studley, Stephen A.; Hayes, J. M.
  • Analytical Chemistry, Vol. 57, Issue 7
  • DOI: 10.1021/ac00284a060

Rapid canopy closure for maize production in the northern US corn belt: Radiation-use efficiency and grain yield
journal, February 1997


Construction of RFLP-based maps of foxtail millet, Setaria italica (L.) P. Beauv.
journal, January 1998

  • Wang, Z. M.; Devos, K. M.; Liu, C. J.
  • Theoretical and Applied Genetics, Vol. 96, Issue 1
  • DOI: 10.1007/s001220050705

Quantitative trait loci associated with natural diversity in water-use efficiency and response to soil drying in Brachypodium distachyon
journal, October 2016


Detection of a quantitative trait locus controlling carbon isotope discrimination and its contribution to stomatal conductance in japonica rice
journal, February 2009

  • Takai, Toshiyuki; Ohsumi, Akihiro; San-oh, Yumiko
  • Theoretical and Applied Genetics, Vol. 118, Issue 7
  • DOI: 10.1007/s00122-009-0990-9

Correlation between carbon isotope discrimination and transpiration efficiency in lines of the C4 species Sorghum bicolor in the glasshouse and the field
journal, January 1998

  • Henderson, S.; Caemmerer, S. von; Farquhar, G. D.
  • Functional Plant Biology, Vol. 25, Issue 1
  • DOI: 10.1071/PP95033

Comparative performance of δ13C, δ18O and δ15N for phenotyping durum wheat adaptation to a dryland environment
journal, January 2013

  • Araus, José Luis; Cabrera-Bosquet, Llorenç; Serret, María Dolores
  • Functional Plant Biology, Vol. 40, Issue 6
  • DOI: 10.1071/FP12254

Using carbon isotope discrimination to select maize (Zea mays L.) inbred lines and hybrids for drought tolerance
journal, October 2007


Physiological and agronomic approaches for improving water-use efficiency in crop plants
journal, June 2019


Components of Water Use Efficiency Have Unique Genetic Signatures in the Model C 4 Grass Setaria
journal, August 2018

  • Feldman, Max J.; Ellsworth, Patrick Z.; Fahlgren, Noah
  • Plant Physiology, Vol. 178, Issue 2
  • DOI: 10.1104/pp.18.00146

Improving water use efficiency in grapevines: potential physiological targets for biotechnological improvement
journal, January 2010


On the Nature of Carbon Isotope Discrimination in C4 Species
journal, January 1983


Mapping Quantitative Trait Loci Underlying Function-Valued Traits Using Functional Principal Component Analysis and Multi-Trait Mapping
journal, November 2015

  • Kwak, Il-Youp; Moore, Candace R.; Spalding, Edgar P.
  • G3: Genes|Genomes|Genetics, Vol. 6, Issue 1
  • DOI: 10.1534/g3.115.024133

Acclimation to low light by C4 maize: implications for bundle sheath leakiness: Maize acclimation to low light
journal, October 2013

  • Bellasio, Chandra; Griffiths, Howard
  • Plant, Cell & Environment, Vol. 37, Issue 5
  • DOI: 10.1111/pce.12194

Carbon and nitrogen winter storage and remobilisation during seasonal flush growth in two-year-old cork oak ( Quercus suber L.) saplings
journal, October 2004

  • Cerasoli, Sofia; Maillard, Pascale; Scartazza, Andrea
  • Annals of Forest Science, Vol. 61, Issue 7
  • DOI: 10.1051/forest:2004058

Improving agricultural water use efficiency in arid and semiarid areas of China
journal, February 2006


The efficiency of C4 photosynthesis under low light conditions: assumptions and calculations with CO2 isotope discrimination
journal, April 2011

  • Ubierna, Nerea; Sun, Wei; Cousins, Asaph B.
  • Journal of Experimental Botany, Vol. 62, Issue 9
  • DOI: 10.1093/jxb/err073

Quantitative trait loci controlling water use efficiency and related traits in Quercus robur L.
journal, August 2007

  • Brendel, Oliver; Le Thiec, Didier; Scotti-Saintagne, Caroline
  • Tree Genetics & Genomes, Vol. 4, Issue 2
  • DOI: 10.1007/s11295-007-0107-z

Potential yield and water-use efficiency benefits in sorghum from limited maximum transpiration rate
journal, January 2005

  • Sinclair, Thomas R.; Hammer, Graeme L.; van Oosterom, Erik J.
  • Functional Plant Biology, Vol. 32, Issue 10
  • DOI: 10.1071/FP05047

Has photosynthetic capacity increased with 80 years of soybean breeding? An examination of historical soybean cultivars: Photosynthesis in historical soybean cultivars
journal, February 2016

  • Koester, Robert P.; Nohl, Brittany M.; Diers, Brian W.
  • Plant, Cell & Environment, Vol. 39, Issue 5
  • DOI: 10.1111/pce.12675

Water-Use Efficiency in Crop Production
journal, January 1984

  • Sinclair, T. R.; Tanner, C. B.; Bennett, J. M.
  • BioScience, Vol. 34, Issue 1
  • DOI: 10.2307/1309424

How can we breed for more water use-efficient sugarcane?
journal, February 2016


QTLs for grain carbon isotope discrimination in field-grown barley
journal, December 2002


Increasing agricultural water use efficiency to meet future food production
journal, December 2000


Leaf-level water use efficiency determined by carbon isotope discrimination in rice seedlings: genetic variation associated with population structure and QTL mapping
journal, February 2009

  • Xu, Yunbi; This, Dominique; Pausch, Roman C.
  • Theoretical and Applied Genetics, Vol. 118, Issue 6
  • DOI: 10.1007/s00122-009-0963-z

Reduced nighttime transpiration is a relevant breeding target for high water-use efficiency in grapevine
journal, July 2016

  • Coupel-Ledru, Aude; Lebon, Eric; Christophe, Angélique
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 32
  • DOI: 10.1073/pnas.1600826113

Enhancing Water Use Efficiency in Irrigated Agriculture
journal, January 2001


Water Use Efficiency as a Constraint and Target for Improving the Resilience and Productivity of C 3 and C 4 Crops
journal, April 2019


Deficit irrigation in grapevine improves water-use efficiency while controlling vigour and production quality
journal, April 2007


Isotopic Composition of Plant Carbon Correlates With Water-Use Efficiency of Wheat Genotypes
journal, January 1984

  • Farquhar, Gd; Richards, Ra
  • Functional Plant Biology, Vol. 11, Issue 6
  • DOI: 10.1071/PP9840539

Leaf stable carbon isotope composition reflects transpiration efficiency in Zea mays
journal, December 2018

  • Twohey, Robert J.; Roberts, Lucas M.; Studer, Anthony J.
  • The Plant Journal, Vol. 97, Issue 3
  • DOI: 10.1111/tpj.14135

Performance and water-use efficiency (single-leaf vs. whole-canopy) of well-watered and half-stressed split-root Lambrusco grapevines grown in Po Valley (Italy)
journal, January 2009

  • Poni, Stefano; Bernizzoni, Fabio; Civardi, Silvia
  • Agriculture, Ecosystems & Environment, Vol. 129, Issue 1-3
  • DOI: 10.1016/j.agee.2008.07.009

Variability of water use efficiency in grapevines
journal, July 2014


Comparative genetic maps of foxtail millet (Setaria italica) and rice (Oryza sativa)
journal, January 1998

  • Devos, K. M.; Wang, Z. M.; Beales, J.
  • Theoretical and Applied Genetics, Vol. 96, Issue 1
  • DOI: 10.1007/s001220050709

Relationship of leaf oxygen and carbon isotopic composition with transpiration efficiency in the C4 grasses Setaria viridis and Setaria italica
journal, June 2017

  • Ellsworth, Patrick Z.; Ellsworth, Patrícia V.; Cousins, Asaph B.
  • Journal of Experimental Botany, Vol. 68, Issue 13
  • DOI: 10.1093/jxb/erx185

Stopping the leaks: new insights into C 4 photosynthesis at low light: C 4 photosynthesis at low light
journal, February 2014


Fine mapping a QTL for carbon isotope composition in tomato
journal, April 2008

  • Xu, Xiangyang; Martin, Bjorn; Comstock, Jonathan P.
  • Theoretical and Applied Genetics, Vol. 117, Issue 2
  • DOI: 10.1007/s00122-008-0767-6

High-throughput Phenotyping and Genomic Selection: The Frontiers of Crop Breeding ConvergeF: High-throughput Phenotyping and Genomic Selection
journal, May 2012

  • Cabrera-Bosquet, Llorenç; Crossa, José; von Zitzewitz, Jarislav
  • Journal of Integrative Plant Biology, Vol. 54, Issue 5
  • DOI: 10.1111/j.1744-7909.2012.01116.x

Bundle-sheath leakiness in C4 photosynthesis: a careful balancing act between CO2 concentration and assimilation
journal, April 2014

  • Kromdijk, J.; Ubierna, N.; Cousins, A. B.
  • Journal of Experimental Botany, Vol. 65, Issue 13
  • DOI: 10.1093/jxb/eru157

The ERECTA gene regulates plant transpiration efficiency in Arabidopsis
journal, July 2005

  • Masle, Josette; Gilmore, Scott R.; Farquhar, Graham D.
  • Nature, Vol. 436, Issue 7052
  • DOI: 10.1038/nature03835

Genetic dissection of cotton physiological responses to arid conditions and their inter-relationships with productivity
journal, February 2004


Water and nitrogen conditions affect the relationships of Δ13C and Δ18O to gas exchange and growth in durum wheat
journal, February 2009

  • Cabrera-Bosquet, Llorenç; Molero, Gemma; Nogués, Salvador
  • Journal of Experimental Botany, Vol. 60, Issue 6
  • DOI: 10.1093/jxb/erp028

How yield relates to ash content, Δ13C and Δ18O in maize grown under different water regimes
journal, September 2009

  • Cabrera-Bosquet, Llorenç; Sánchez, Ciro; Araus, José Luis
  • Annals of Botany, Vol. 104, Issue 6
  • DOI: 10.1093/aob/mcp229

Two new organic reference materials for δ 13 C and δ 15 N measurements and a new value for the δ 13 C of NBS 22 oil : Organic reference materials for
journal, October 2003

  • Qi, Haiping; Coplen, Tyler B.; Geilmann, Heike
  • Rapid Communications in Mass Spectrometry, Vol. 17, Issue 22
  • DOI: 10.1002/rcm.1219

Short-term thermal photosynthetic responses of C4 grasses are independent of the biochemical subtype
journal, September 2017

  • Sonawane, Balasaheb V.; Sharwood, Robert E.; von Caemmerer, Susanne
  • Journal of Experimental Botany, Vol. 68, Issue 20
  • DOI: 10.1093/jxb/erx350

High-precision continuous-flow isotope ratio mass spectrometry
journal, January 1997


Transpiration efficiency and carbon-isotope discrimination of grapevines grown under well-watered conditions in either glasshouse or vineyard
journal, October 2001


Stable Carbon Isotope Discrimination Is under Genetic Control in the C4 Species Maize with Several Genomic Regions Influencing Trait Expression
journal, November 2013

  • Gresset, S.; Westermeier, P.; Rademacher, S.
  • PLANT PHYSIOLOGY, Vol. 164, Issue 1
  • DOI: 10.1104/pp.113.224816

Quantitative trait loci for carbon isotope discrimination are repeatable across environments and wheat mapping populations
journal, September 2008

  • Rebetzke, G. J.; Condon, A. G.; Farquhar, G. D.
  • Theoretical and Applied Genetics, Vol. 118, Issue 1
  • DOI: 10.1007/s00122-008-0882-4

Carbon Isotope Discrimination and Photosynthesis
journal, June 1989

  • Farquhar, G. D.; Ehleringer, J. R.; Hubick, K. T.
  • Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 40, Issue 1, p. 503-537
  • DOI: 10.1146/annurev.pp.40.060189.002443

GENETICS OF DROUGHT ADAPTATION IN ARABIDOPSIS THALIANA II. QTL ANALYSIS OF A NEW MAPPING POPULATION, KAS-1 × TSU-1
journal, December 2008


Transpiration efficiency: new insights into an old story
journal, March 2014

  • Vadez, Vincent; Kholova, Jana; Medina, Susan
  • Journal of Experimental Botany, Vol. 65, Issue 21
  • DOI: 10.1093/jxb/eru040