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Stylar canal architecture of maize is not an indicator of resistance to Fusarium verticillioides infection

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Abstract

Fusarium verticillioides causes Fusarium ear rot (FER) of maize and contaminates the grain with mycotoxins called fumonisins. Structural barriers that prevent infection include a closed stylar canal of kernels, which has been suggested to contribute to resistance to FER. In this study, the stylar canal architecture of nine maize inbred lines, characterised for their response to F. verticillioides, was evaluated using scanning electron microscopy. The stylar canal of ovaries, sampled at 1–2 weeks before pollination, and maturing kernels sampled at approximately 1 month after self-pollination, were evaluated. Three inbred lines, CML 390 (highly resistant), RO 544 W (intermediately resistant) and R2565y (susceptible), had ovaries predominantly with closed stylar canals, with 92, 95 and 64.3% of the canals viewed as closed, respectively. Other highly resistant (CML 444, VO 617Y-2 and US 2540 W), intermediately resistant (RO 549 W) and susceptible (R119W and I137tnW) inbred lines displayed a mostly open stylar canal prior to pollination. The stylar canals of all inbred lines were mostly closed 1 month after pollination (90.3–100%). No significant association was found between stylar canal architecture and the FER-resistance status of the maize lines evaluated for ovaries and maturing maize kernels (P > 0.05). The results of the study suggest that the stylar canal architecture may facilitate fungal ingress but does not play a pivotal role in resistance to F. verticillioides.

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References

  • Beekrum, S., Govinden, R., Padayachee, T., & Odhav, B. (2003). Naturally occurring phenols: A detoxification strategy for fumonisin B1. Food Additives and Contaminants, 20(5), 490–493. https://doi.org/10.1080/0265203031000098678.

    Article  CAS  PubMed  Google Scholar 

  • Blandino, M., & Reyneri, A. (2008). Effect of maize hybrid maturity and grain hardness on fumonisin and zearalenone contamination. Italian Journal of Agronomy, 3(2), 107–117. https://doi.org/10.4081/ija.2008.107.

    Article  Google Scholar 

  • Bluhm, B. H., & Woloshuk, C. P. (2005). Amylopectin induces fumonisin B1 production by Fusarium verticillioides during colonization of maize kernels. Molecular Plant-Microbe Interactions, 18(12), 1333–1339. https://doi.org/10.1094/MPMI-18-1333.

    Article  CAS  PubMed  Google Scholar 

  • Cao, A., Santiago, R., Ramos, A. J., Marín, S., Reid, L. M., & Butrón, A. (2013). Environmental factors related to fungal infection and fumonisin accumulation during the development and drying of white maize kernels. International Journal of Food Microbiology, 164(1), 15–22. https://doi.org/10.1016/j.ijfoodmicro.2013.03.012.

    Article  CAS  PubMed  Google Scholar 

  • Chen, J., Ding, J., Li, H., Li, Z., Sun, X., Li, J., Wang, R., Dai, X., Dong, H., Song, W., Chen, W., Xia, Z., & Wu, J. (2012). Detection and verification of quantitative trait loci for resistance to Fusarium ear rot in maize. Molecular Breeding, 30(4), 1649–1656. https://doi.org/10.1007/s11032-012-9748-1.

    Article  CAS  Google Scholar 

  • Chisholm, S. T., Coaker, G., Day, B., & Staskawicz, B. J. (2006). Host-microbe interactions: Shaping the evolution of the plant immune response. Cell, 124(4), 803–814. https://doi.org/10.1016/j.cell.2006.02.008.

    Article  CAS  PubMed  Google Scholar 

  • Duncan, K. E., & Howard, R. J. (2010). Biology of maize kernel infection by Fusarium verticillioides. Molecular Plant-Microbe Interactions, 23(1), 6–16. https://doi.org/10.1094/MPMI-23-1-0006.

    Article  CAS  PubMed  Google Scholar 

  • Flett, B. C., & van Rensburg, J. B. J. (1992). Effect of Busseola fusca on the incidence of maize ear rot caused by Fusarium moniliforme and Stenocarpella maydis. South African Journal of Plant and Soil, 9(4), 177–179. https://doi.org/10.1080/02571862.1992.10634625.

    Article  Google Scholar 

  • Hoenisch, R. W., & Davis, R. M. (1994). Relationship between kernel pericarp thickness and susceptibility to Fusarium ear rot in field corn. Plant Disease, 78(5), 517–519. https://doi.org/10.1094/PD-78-0517.

    Article  Google Scholar 

  • Ivić, D., Čabrić, M., Palaveršić, B., & Cvjetković, B. (2008). No correlation between pericarp thickness and Fusarium ear rot (Fusarium verticillioides) in Croatian maize hybrids and lines. Maydica, 53(3–4), 297–301.

    Google Scholar 

  • Jurado, M., Marín, P., Magan, N., & González-Jaén, M. T. (2008). Relationship between solute and matric potential stress, temperature, growth, and FUM1 gene expression in two 39 Fusarium verticillioides strains from Spain. Applied and Environmental Microbiology, 74(7), 2032–2036. https://doi.org/10.1128/AEM.02337-07.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, H., & Woloshuk, C. P. (2008). Role of AREA, a regulator of nitrogen metabolism, during colonization of maize kernels and fumonisin biosynthesis in Fusarium verticillioides. Fungal Genetics and Biology, 45(6), 947–953. https://doi.org/10.1016/j.fgb.2008.03.007.

  • Lanubile, A., Luca, P., & Adriano, M. (2010). Differential gene expression in kernels and silks of maize lines with contrasting levels of ear rot resistance after Fusarium verticillioides infection. Journal of Plant Physiology, 167(16), 1398–1406. https://doi.org/10.1016/j.jplph.2010.05.015.

    Article  CAS  PubMed  Google Scholar 

  • Lanubile, A., Maschietto, V., Borrelli, V. M., Stagnati, L., Logrieco, A. F., & Marocco, A. (2017). Molecular basis of resistance to Fusarium ear rot in maize. Frontiers in Plant Science, 8, article 1774. https://doi.org/10.3389/fpls.2017.01774.

  • Li, Z., Ding, J., Wang, R., Chen, J., Sun, X., Chen, W., et al. (2011). A new QTL for resistance to Fusarium ear rot in maize. Journal of Applied Genetics, 52(4), 403–406.

    Article  PubMed  Google Scholar 

  • Li, H., Wu, Y., Zhao, Y., Hu, X., Chang, J., Wang, Q., Dong P., Zhang M., Li C. (2016). Differential morphology and transcriptome profile between the incompletely fused carpels ovary and its wild-type in maize. Scientific Reports, 6, article 32652. https://doi.org/10.1038/srep32652.

  • Links, S. (2019). Phenotypic, physico-chemical and genetic responses of maize associated with resistance to Fusarium verticillioides. MSc thesis, University of Stellenbosch, Stellenbosch, South Africa.

  • Links, S., van Zyl, K., Cassiem, A., Flett, B. C., Viljoen, A., & Rose, L. J. (2020). The association of maize characteristics with resistance to Fusarium verticillioides and fumonisin accumulation in commercial maize cultivars. World Mycotoxin Journal, 13(3), 1–14.

    Article  Google Scholar 

  • Löffler, M., Kessel, B., Ouzunova, M., & Miedaner, T. (2010). Population parameters for resistance to Fusarium graminearum and Fusarium verticillioides ear rot among large sets of early, mid-late and late maturing European maize (Zea mays L.) inbred lines. Theoretical and Applied Genetics, 120(5), 1053–1062. https://doi.org/10.1007/s00122-009-1233-9.

    Article  PubMed  Google Scholar 

  • Mesterházy, Á., Lemmens, M., & Reid, L. M. (2012). Breeding for resistance to ear rots caused by Fusarium spp. in maize - a review. Plant Breeding, 131(1), 1–19. https://doi.org/10.1111/j.1439-0523.2011.01936.x.

    Article  Google Scholar 

  • Miller, E. C. (1919). Development of the pistillate spikelet and fertilization in Zea mays L. Journal of Agricultural Research, 18(5), 255–266.

    Google Scholar 

  • Munkvold, G. P., & Carlton, W. M. (1997). Influence of inoculation method on systemic Fusarium moniliforme infection of maize plants grown from infected seeds. Plant Disease, 81(2), 211–216. https://doi.org/10.1094/PDIS.1997.81.2.211.

    Article  CAS  PubMed  Google Scholar 

  • Murillo-Williams, A., & Munkvold, G. P. (2008). Systemic infection by Fusarium verticillioides in maize plants grown under three temperature regimes. Plant Disease, 92(12), 1695–1700. https://doi.org/10.1094/PDIS-92-12-1695.

    Article  CAS  PubMed  Google Scholar 

  • Nickerson, N. H. (1954). Morphological analysis of the maize ear. American Journal of Botany, 41(2), 87–92. https://doi.org/10.2307/2439311.

    Article  Google Scholar 

  • Okoth, S., Rose, L. J., Ouko, A., Beukes, I., Sila, H., Mouton, M., Flett, B. C., Makumbi, D., & Viljoen, A. (2017a). Field evaluation of resistance to aflatoxin accumulation in maize inbred lines in Kenya and South Africa. Journal of Crop Improvement, 31(6), 862–878. https://doi.org/10.1080/15427528.2017.1391915.

    Article  CAS  Google Scholar 

  • Okoth, S., Rose, L. J., Ouko, A., Nakisani, N. E. I., Sila, H. & Viljoen, A. (2017b). Assessing genotype by environment interactions in Aspergillus ear rot and preharvest aflatoxin accumulation in maize inbred lines. Agronomy, 7(4), article 86. https://doi.org/10.3390/agronomy7040086

  • Oren, L., Ezrati, S., Cohen, D., & Sharon, A. (2003). Early events in the Fusarium verticillioides-maize interaction characterized by using a green fluorescent protein-expressing transgenic isolate. Applied and Environmental Microbiology, 69(3), 1695–1701. https://doi.org/10.1128/AEM.69.3.1695.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parsons, M. W., & Munkvold, G. P. (2010). Associations of planting date, drought stress, and insects with Fusarium ear rot and fumonisin B1 contamination in California maize. Food Additives and Contaminants, 27(5), 591–607. https://doi.org/10.1080/19440040903456337.

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Brito, D., Jeffers, D., González-de-León, D., Khairallah, M., Cortés-Cruz, M., Velázquez-Cardelas, G., et al. (2001). QTL mapping of Fusarium moniliforme ear rot resistance in highland maize, Mexico. Agrociencia, 35(2), 181–196.

    Google Scholar 

  • Picot, A., Barreau, C., Pinson-Gadais, L., Piraux, F., Caron, D., Lannou, C., & Richard-Forget, F. (2011). The dent stage of maize kernels is the most conducive for fumonisin biosynthesis under field conditions. Applied and Environmental Microbiology, 77(23), 8382–8390. https://doi.org/10.1128/AEM.05216-11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reid, L. M., Woldemariam, T., Zhu, X., Stewart, D. W., & Schaafsma, A. W. (2002). Effect of inoculation time and point of entry on disease severity in Fusarium graminearum, Fusarium verticillioides, or Fusarium subglutinans inoculated maize ears. Canadian Journal of Plant Pathology, 24(2), 162–167. https://doi.org/10.1080/07060660309506991.

    Article  Google Scholar 

  • Rose, L. J., Mouton, M., Beukes, I., Flett, B. C., van der Vyver, C., & Viljoen, A. (2016). Multi-environment evaluation of maize inbred lines to Fusarium ear rot and fumonisins. Plant Disease, 100(10), 2134–2144.

    Article  CAS  PubMed  Google Scholar 

  • Rose, L. J., Okoth, S., Beukes, I., Mouton, M., Flett, B. C., Makumbi, D., et al. (2017). Determining resistance to Fusarium verticillioides and fumonisin accumulation in maize inbred lines resistant to Aspergillus flavus and aflatoxins. Euphytica, 213, article 93. https://doi.org/10.1007/s10681-017-1883-7.

  • Sacco, M. A., & Moffett, P. (2009). Disease resistance genes: Form and function. In K. Bouarab, N. Brisson, & F. Daayf (Eds.), Molecular plant microbe interactions (pp. 94–141). CABI.

  • Sampietro, D. A., Vattuone, M. A., Presello, D. A., Fauguel, C. M., & Catalán, C. A. N. (2009). The pericarp and its surface wax layer in maize kernels as resistance factors to fumonisin accumulation by Fusarium verticillioides. Crop Protection, 28(2), 196–200. https://doi.org/10.1016/j.cropro.2008.09.010.

    Article  CAS  Google Scholar 

  • Sampietro, D. A., Fauguel, C. M., Vattuone, M. A., Presello, D. A., & Catalán, C. A. N. (2013). Phenylpropanoids from maize pericarp: Resistance factors to kernel infection and fumonisin accumulation by Fusarium verticillioides. European Journal of Plant Pathology, 135(1), 105–113. https://doi.org/10.1007/s10658-012-0069-3.

    Article  CAS  Google Scholar 

  • Scott, G. E., & King, S. B. (1984). Site of action of factors for resistance to Fusarium moniliforme in maize. Plant Disease, 68(9), 804–806.

    Article  Google Scholar 

  • Shaikh, A. (2020). Fusarium verticillioides infection and fumonisin production during maize kernel maturation. , University of Stellenbosch, Stellenbosch, South Africa.

  • Small, I. M., Flett, B. C., Marasas, W. F. O., Mcleod, A., Stander, M. A., & Viljoen, A. (2012). Resistance in maize inbred lines to Fusarium verticillioides and fumonisin accumulation in South Africa. Plant Disease, 96(6), 881–888.

    Article  CAS  PubMed  Google Scholar 

  • Smith, J. E., Lay, J. O., & Bluhm, B. H. (2012). Metabolic fingerprinting reveals a new genetic 46 linkage between ambient pH and metabolites associated with desiccation tolerance in Fusarium verticillioides. Metabolomics, 8(3), 376–385. https://doi.org/10.1007/s11306-011-0322-3.

    Article  CAS  Google Scholar 

  • Van Zyl, K. (2015). Resistance in maize to infection and toxin production by Fusarium verticillioides. , University of Stellenbosch, Stellenbosch, South Africa.

  • Warfield, C. Y., & Davis, R. M. (1996). Importance of the husk covering on the susceptibility of corn hybrids to Fusarium ear rot. Plant Disease, 80(2), 208–210. https://doi.org/10.1094/PD-80-0208.

    Article  Google Scholar 

  • Zila, C., Samayoa, L., Santiago, R., Butrόn, A., & Holland, J. (2013). A genome-wide association study reveals genes associated with Fusarium ear rot resistance in a maize core diversity panel. Investigation, 3(11), 2095–2104. https://doi.org/10.1534/g3.113.007328.

    Article  CAS  Google Scholar 

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Acknowledgements

We wish to express our sincere gratitude and appreciation to the following people: Ms. M. Frazenburg (Central Analytical Facility, Stellenbosch University) for assistance with microscopy imaging and Ms. M. Van Der Rijst (Agriculture Research Council-Infruitec) for the statistical analyses.

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Funding

This study was funded by the South African Maize Trust and the National Research Foundation (NRF) of South Africa.

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All authors contributed to the conception and study design. Material preparation, data collection and analysis were performed by M. van Dyk. The first draft of the manuscript was written by M. van Dyk and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Lindy Joy Rose.

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van Dyk, M., Viljoen, A. & Rose, L.J. Stylar canal architecture of maize is not an indicator of resistance to Fusarium verticillioides infection. Eur J Plant Pathol 161, 475–481 (2021). https://doi.org/10.1007/s10658-021-02327-3

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