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Paternal leakage inheritance and a fitness cost are associated with the chloroplastic psbA gene controlled metribuzin tolerance in lentil (Lens culinaris)

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Abstract

Reciprocal F1, F2 and F3 populations of lentil (Lens culinaris Medik.) were developed by crossing between lines, with a chloroplastic psbA gene mutation conferring tolerance to the photosystem II inhibitor herbicide metribuzin, and sensitive parent PBA Flash, to understand the genetic control of the herbicide tolerance. Additionally, reciprocal BC1F2 populations were developed to identify any fitness penalty associated with the metribuzin tolerance. Phenotyping and genotyping results of the F1, F2, and F3 populations identified a predominantly maternal inheritance pattern, but with a level of paternal leakage. Paternal leakage occurred in approximately 20% of F1 phenotypes, when including lines showing heteroplasmy (the existence of maternal and paternal chloroplasts within an individual). Field experiments with BC1F2 and BC1F3 lines confirmed this biparental inheritance pattern. Grain yield was reduced by 20–40% in metribuzin tolerant backcrossed lines compared with sensitive lines. Net assimilation rate at the onset of anthesis and plant dry weight at mid anthesis and maturity were also reduced in the tolerant lines suggesting reduced photosynthetic efficiency associated with the metribuzin tolerance results in lower dry weight and grain yield in the tolerant lines. The mode of inheritance and associated yield penalty of the tolerance trait will complicate its introgression in lentil breeding programs. However, the high level of tolerance and unique weed control benefits of this trait suggest that this form of metribuzin tolerance in lentil, which is similar to triazine tolerant canola (Brassica napus L.), could be adopted.

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Availability of data and material

The translated amino acid sequence from M009, M043 and the susceptible parent PBA Flash are available in the GenBank database as MH681284, MH681285 and MH681286. All data from this research is deposited with the University of Adelaide data depository and can be made available upon request.

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Acknowledgements

The Grains Research Development Corporation (GRDC), the South Australian Research and Development Institute (SARDI), the University of Adelaide, the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Saskatchewan Pulse Growers (SPG) provided financial support for this study. The Plant Accelerator, Australian Plant Phenomics Facility, a research facility funded by the National Collaborative Research Infrastructure Strategy (NCRIS). Technical assistance and input were provided by Shi Ying Yang and Ruwan Lenorage of the University of Adelaide; Jamus Stonur, Kathy Fischer, Henk Venter, John Nairn, Phil Rundle, Brooke Schofield. Tim Jenkins, Parminder Sidhu of SARDI; and Robert Stonehouse, Vladimir Pajic, Kendra Meier, Brent Barlow, Devini De Silva, Chandra Bandara and Adam Harrison from the University of Saskatchewan. Dr Richard Jarret, University of Adelaide provided valuable contribution to the statistical analysis of the fitness cost field studies. No conflicts of interest have been declared.

Funding

The Grains Research Development Corporation (GRDC), the South Australian Research and Development Institute (SARDI), the University of Adelaide, the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Saskatchewan Pulse Growers (SPG) provided financial support for this study. The Plant Accelerator, Australian Plant Phenomics Facility, a research facility funded by the National Collaborative Research Infrastructure Strategy (NCRIS).

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Authors and Affiliations

  1. School of Agriculture, Food and Wine, The University of Adelaide, Adelaide, SA, 5064, Australia

    Larn S. McMurray, Christopher Preston, Isabel Munoz-Santa & Jeffrey G. Paull

  2. South Australian Research and Development Institute, PO Box 822, Clare, SA, 5453, Australia

    Larn S. McMurray, Dili Mao & Simon Michelmore

  3. Department of Plant Sciences/Crop Development Centre, University of Saskatchewan, Saskatoon, SK, S7N 5A8, Canada

    Albert Vandenberg & Kirstin E. Bett

  4. Department of Statistics and Operations Research, University of Valencia, 46100, Valencia, Spain

    Isabel Munoz-Santa

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  1. Larn S. McMurray
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Correspondence to Larn S. McMurray.

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McMurray, L.S., Preston, C., Vandenberg, A. et al. Paternal leakage inheritance and a fitness cost are associated with the chloroplastic psbA gene controlled metribuzin tolerance in lentil (Lens culinaris). Euphytica 217, 103 (2021). https://doi.org/10.1007/s10681-021-02841-9

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