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The ERECTA gene regulates plant transpiration efficiency in Arabidopsis

Abstract

Assimilation of carbon by plants incurs water costs. In the many parts of the world where water is in short supply, plant transpiration efficiency, the ratio of carbon fixation to water loss, is critical to plant survival, crop yield and vegetation dynamics1. When challenged by variations in their environment, plants often seem to coordinate photosynthesis and transpiration2, but significant genetic variation in transpiration efficiency has been identified both between and within species3,4. This has allowed plant breeders to develop effective selection programmes for the improved transpiration efficiency of crops5, after it was demonstrated that carbon isotopic discrimination, Δ, of plant matter was a reliable and sensitive marker negatively related to variation in transpiration efficiency3,4,6. However, little is known of the genetic controls of transpiration efficiency. Here we report the isolation of a gene that regulates transpiration efficiency, ERECTA. We show that ERECTA, a putative leucine-rich repeat receptor-like kinase (LRR-RLK)7,8 known for its effects on inflorescence development7,9, is a major contributor to a locus for Δ on Arabidopsis chromosome 2. Mechanisms include, but are not limited to, effects on stomatal density, epidermal cell expansion, mesophyll cell proliferation and cell–cell contact.

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Figure 1: ERECTA , a transpiration efficiency gene.
Figure 2: ERECTA regulates leaf gas exchange.
Figure 3: Leaf anatomical features contributing to the effects of ERECTA on transpiration efficiency.
Figure 4: ERECTA improved transpiration efficiency under both well-watered and drought conditions.

References

  1. Boyer, J. S. Plant productivity and environment. Science 218, 443–448 (1982)

    ADS  CAS  Article  Google Scholar 

  2. Wong, S. C., Cowan, I. R. & Farquhar, G. D. Stomatal conductance correlates with photosynthetic capacity. Nature 282, 424–426 (1979)

    ADS  Article  Google Scholar 

  3. Farquhar, G. D., Ball, M. C., von Caemmerer, S. & Roksandic, Z. Effect of salinity and humidity on δ13C values of halophytes—evidence of diffusional isotope fractionation determined by the ratio of intercellular/atmospheric partial pressure of CO2 under different environmental conditions. Oecologia 52, 121–124 (1982)

    ADS  CAS  Article  Google Scholar 

  4. Farquhar, G. D. & Richards, R. A. Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust. J. Plant Physiol. 11, 539–552 (1984)

    CAS  Google Scholar 

  5. Rebetzke, G. J., Condon, A. G., Richards, R. A. & Farquhar, G. D. Selection for reduced carbon isotope discrimination increases aerial biomass and grain yield of rain fed bread wheat. Crop Sci. 42, 739–745 (2002)

    Article  Google Scholar 

  6. Farquhar, G. D., O'Leary, M. H. & Berry, J. A. On the relationship between carbon isotopic discrimination and intercellular carbon dioxide concentration in leaves. Aust. J. Plant Physiol. 9, 121–137 (1982)

    CAS  Google Scholar 

  7. Torii, K. U. et al. The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8, 735–746 (1996)

    CAS  Article  Google Scholar 

  8. Lease, K. A., Lau, N. Y., Schuster, R. A., Torii, K. U. & Walker, J. C. Receptor serine/threonine protein kinases in signalling: analysis of the ERECTA receptor-like kinase of Arabidopsis thaliana. New Phytol. 151, 133–143 (2001)

    CAS  Article  Google Scholar 

  9. Bowman, J. in Arabidopsis: An atlas of morphology and development (ed. Bowman, J.) (Springer, New York, 1994)

    Book  Google Scholar 

  10. Masle, J., Shin, J. S. & Farquhar, G. D. in Perspectives of Plant Carbon and Water Relations from Stable Isotopes (eds Ehleringer, J., Hall, A. E. & Farquhar, G. D.) 371–386 (Academic, New York, 1993)

    Book  Google Scholar 

  11. Lister, C. & Dean, C. Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J. 4, 745–750 (1993)

    CAS  Article  Google Scholar 

  12. Martin, B., Nienhuis, J., King, G. & Schaefer, A. Restriction fragment length polymorphisms associated with water-use efficiency in tomato. Science 243, 1725–1728 (1989)

    ADS  CAS  Article  Google Scholar 

  13. Thumma, B. R. et al. Identification of causal relationships among traits related to drought resistance in Stylosanthes scabra using QTL analysis. J. Exp. Bot. 52, 203–214 (2001)

    CAS  Article  Google Scholar 

  14. Zhu, Y., Kuanhung, R. L., Huang, Y., Tauer, C. G. & Martin, B. A cDNA from tomato (Lycopersicon pennellii) encoding ribulose-1,5-bisphosphate carboxylase/oxygenase activase (accession No. AF037361) (PGR98–053). Plant Gene Register 116, 1603 (1998)

    Google Scholar 

  15. Shpak, E. D., Lakeman, M. B. & Torii, K. U. Dominant-negative receptor uncovers redundancy in the Arabidopsis ERECTA leucine-rich repeat receptor-like kinase signalling pathway that regulates organ shape. Plant Cell 15, 1095–1110 (2003)

    CAS  Article  Google Scholar 

  16. Godiard, L. et al. ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. Plant J. 36, 353–365 (2003)

    CAS  Article  Google Scholar 

  17. Farquhar, G. D., von Caemmerer, S. & Berry, J. A. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90 (1980)

    CAS  Article  Google Scholar 

  18. Douglas, S. J., Chuck, G., Dengler, R. E., Pelecanda, L. & Riggs, C. D. KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell 14, 547–558 (2002)

    CAS  Article  Google Scholar 

  19. Shpak, E. D., Berthiaume, C. T., Hill, E. J. & Torii, K. U. Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131, 1491–1501 (2004)

    CAS  Article  Google Scholar 

  20. Nadeau, J. A. & Sachs, F. D. in The Arabidopsis Book (eds Somerville, C. & Meyerowitz, E.) 1–28 http://www.aspb.org/publications/arabidopsis/ (American Society of Plant Biologists, Rockville, Maryland, 2002)

    Google Scholar 

  21. Farquhar, G. D. & Raschke, K. On the resistance to transpiration of the sites of evaporation within the leaf. Plant Physiol. 61, 1000–1005 (1978)

    CAS  Article  Google Scholar 

  22. Yokoyama, R., Takahashi, T., Kato, A., Torii, K. U. & Komeda, Y. The Arabidopsis ERECTA gene is expressed in the shoot apical meristem and organ primordia. Plant J. 15, 301–310 (1998)

    CAS  Article  Google Scholar 

  23. Xu, L. et al. Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130, 4097–4107 (2003)

    CAS  Article  Google Scholar 

  24. Lander, E. S. & Botstein, D. Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121, 185–199 (1989)

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Zeng, Z.-B. Precision mapping of Quantitative Trait Loci. Genetics 136, 1457–1468 (1994)

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Basten, C., Weir, B. & Zeng, Z.-B. QTL Cartographer (North Carolina State Univ., Raleigh, North Carolina, 2000)

    Google Scholar 

  27. Loudet, O., Chaillou, S., Camilleri, C., Bouchez, D. & Daniel-Vedele, F. Bay-0 x Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis. Theor. Appl. Genet. 104, 1173–1184 (2002)

    CAS  Article  Google Scholar 

  28. von Caemmerer, S. & Farquhar, G. D. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387 (1981)

    CAS  Article  Google Scholar 

  29. Masle, J., Hudson, G. S. & Badger, M. R. Effects of ambient CO2 concentration on growth and nitrogen use in tobacco (Nicotiana tabacum) plants transformed with an antisense gene to the small subunit of Ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol. 103, 1075–1088 (1993)

    CAS  Article  Google Scholar 

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Acknowledgements

We thank K. Torii for the pKUT196 plasmid, T. Baskin for Coler105 seeds, and S. May, C. Somerville, S. C. Wong, R. Jost and O. Berkowitz for helpful discussions, encouragement and/or comments on the manuscript.

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Correspondence to Josette Masle.

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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figure S1

Relative abundance of ERECTA transcripts in several independent gentamycin resistant T3 transgenic lines (TEReri) obtained by complementation of erecta mutants Coler105 (null mutant), Coler2, and Ler with Col-0 ERECTA. (PDF 332 kb)

Supplementary Figure S2

Phylogram of ERECTA and ERECTA-like genes based on analysis of sequence homology with Arabidopsis AtER and ATERL proteins. ERECTA homologues are identified in a number of C3 and C4, dicot and monocot species, including major crop species. (PDF 310 kb)

Supplementary Table S1

Characteristics of TE1 locus in four different experiments. TE1 was identified by QTL analysis of 100 F9 Recombinant Inbred Lines derived from a cross between Col-4 and Ler. (DOC 33 kb)

Supplementary Table S2

Comparison of carbon isotope discrimination, δ, in 3 erecta mutants and several independent T3 transgenic lines complemented with the Col-0 ERECTA allele. (DOC 50 kb)

Supplementary Methods

This file contains additional methods used in the study, including the determination of carbon isotope composition and discrimination, the relationship between δ and TE, mutant complementation and real-time quantitative PCR assays. (DOC 30 kb)

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Masle, J., Gilmore, S. & Farquhar, G. The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436, 866–870 (2005). https://doi.org/10.1038/nature03835

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