Sequential breakdown of the complex Cf-9 leaf mould resistance locus in tomato by Fulvia fulva

de la Rosa, S.; Schol, C. R.; Peregrina, A. R.; Winter, D. J.; Hilgers, A. M.; Maeda, K.; Iida, Y.; Tarallo, M.; Jia, R.; Beenen, H. G.; Rocafort, M.; de Wit, P. J. G. M.; Bowen, J. K.; Bradshaw, R. E.; Joosten, M. H. A. J.; Bai, Y.; Mesarich, C. H.

doi:10.1101/2023.08.27.554972

bioRxiv · 10.1101/2023.08.27.554972

Sequential breakdown of the complex Cf-9 leaf mould resistance locus in tomato by Fulvia fulva

de la Rosa, S.·Schol, C. R.·Peregrina, A. R.·Winter, D. J.·Hilgers, A. M.·Maeda, K.·Iida, Y.·Tarallo, M.·Jia, R.·Beenen, H. G.·Rocafort, M.·de Wit, P. J. G. M.·Bowen, J. K.·Bradshaw, R. E.·Joosten, M. H. A. J.·Bai, Y.·Mesarich, C. H.

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Abstract

O_LILeaf mould, caused by Fulvia fulva, is a devastating disease of tomato plants. In many commercial tomato cultivars, resistance to this disease is governed by the Cf-9 locus, which comprises five paralogous genes (Cf-9A-9E) that encode receptor-like proteins. Two of these proteins contribute to resistance: Cf-9C recognizes the previously identified F. fulva effector Avr9 and provides resistance during all plant growth stages, while Cf-9B recognises the yet-unidentified F. fulva effector Avr9B and provides mature plant resistance only. In recent years, F. fulva strains have emerged that have overcome the Cf-9 locus, with Cf-9C circumvented through Avr9 deletion. To understand how Cf-9B is circumvented, we set out to identify Avr9B. C_LIO_LIComparative genomics, in planta transient expression assays and gene complementation experiments were used to identify Avr9B, while gene sequencing was used to assess Avr9B allelic variation across a worldwide strain collection. C_LIO_LIA strict correlation between Avr9 deletion and resistance-breaking mutations in Avr9B was observed in strains recently collected from Cf-9 cultivars, whereas Avr9 deletion but no mutations in Avr9B were observed in older strains. C_LIO_LIThis research showcases how F. fulva has evolved to sequentially break down the two functional resistance genes of the complex Cf-9 locus and highlights that this locus now has limited value for controlling leaf mould disease in worldwide commercial tomato production. C_LI

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de la Rosa, S., Schol, C. R., Peregrina, A. R., Winter, D. J., Hilgers, A. M., Maeda, K., Iida, Y., Tarallo, M., Jia, R., Beenen, H. G., Rocafort, M., de Wit, P. J. G. M., Bowen, J. K., Bradshaw, R. E., Joosten, M. H. A. J., Bai, Y., Mesarich, C. H.. 2023-08-27. Sequential breakdown of the complex Cf-9 leaf mould resistance locus in tomato by Fulvia fulva. https://doi.org/10.1101/2023.08.27.554972

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