Phenotypic characterisation and evaluation of resistance to Fusarium ear rot, fumonisin contamination and agronomic traits in a collection of maize landraces
Lorenzo Stagnati A B # , Alessandra Lanubile A B # * , Giovanna Soffritti A , Paola Giorni A , Graziano Rossi C , Adriano Marocco A B and Matteo Busconi A BA
B
C
Handling Editor: Zed Rengel
Abstract
Maize is a major crop in Italy and is constantly affected by the fungus Fusarium verticillioides, producing ear rot and grain contamination by fumonisins. Finding new genotypes resistant to Fusarium infection is an important goal for the improvement of maize cultivation.
The objective of this work was to test a collection of 33 traditional landraces from the Emilia-Romagna (Italy) region for Fusarium ear rot (FER) severity, fumonisin content, and their agronomic performance.
Primary ears were artificially inoculated with a toxigenic strain of F. verticillioides in a 2-year experimental trial. The landrace ‘Nostrano di Storo’ and a commercial hybrid of FAO maturity class 300 were also included and used as comparisons representing a well-known and highly valued landrace and a modern flint hybrid, respectively.
The collection showed great phenotypic variability for all the agronomic traits assessed and responded differently to the Fusarium infection with percentages of FER ranging from 6.6% to 49.3%, and fumonisins from 4.3 mg/kg to 34.5 mg/kg. Thirteen and six landraces displayed FER percentages and fumonisin content very similar to the hybrid, respectively. Moreover, eight landraces exhibited grain yield values comparable to the hybrid. Interestingly, Va221, Va227 and EMR03 showed the best combination among these three traits.
This local material can be considered suitable for breeding purposes targeting the development of FER and fumonisin resistant germplasm.
The collection may represent a resource for future research aimed at evaluating the response to multiple pathogens and their associated mycotoxins.
Keywords: agrobiodiversity, ear morphology, Emilia-Romagna region, fumonisins, Fusarium verticillioides, grain yield, kernel type, maize germplasm.
References
Ardenghi NMG, Rossi G, Guzzon F (2018) Back to beaked: Zea mays subsp. mays Rostrata Group in northern Italy, refugia and revival of open-pollinated maize landraces in an intensive cropping system. PeerJ 6, e5123.
| Crossref | Google Scholar | PubMed |
Arteaga MC, Moreno-Letelier A, Mastretta-Yanes A, Vázquez-Lobo A, Breña-Ochoa A, Moreno-Estrada A, Eguiarte LE, Piñero D (2016) Genomic variation in recently collected maize landraces from Mexico. Genomics Data 7, 38-45.
| Crossref | Google Scholar | PubMed |
Barcaccia G, Lucchin M, Parrini P (2003) Characterization of a flint maize (Zea mays var. indurata) Italian landrace, II. Genetic diversity and relatedness assessed by SSR and Inter-SSR molecular markers. Genetic Resources and Crop Evolution 50, 253-271.
| Crossref | Google Scholar |
Bernardi J, Stagnati L, Lucini L, Rocchetti G, Lanubile A, Cortellini C, De Poli G, Busconi M, Marocco A (2018) Phenolic profile and susceptibility to Fusarium infection of pigmented maize cultivars. Frontiers in Plant Science 9, 1189.
| Crossref | Google Scholar | PubMed |
Bonciarelli F (1961) Studio agronomico comparato delle popolazioni umbre di mais. Maydica 6, 35-61.
| Google Scholar |
Brandolini A, Brandolini A (2009) Maize introduction, evolution and diffusion in Italy. Maydica 54, 233-242.
| Google Scholar |
Cassani E, Puglisi D, Cantaluppi E, Landoni M, Giupponi L, Giorgi A, Pilu R (2017) Genetic studies regarding the control of seed pigmentation of an ancient European pointed maize (Zea mays L.) rich in phlobaphenes: the “Nero Spinoso” from the Camonica valley. Genetic Resources and Crop Evolution 64, 761-773.
| Crossref | Google Scholar |
Centro di Riferimento per l’Agricoltura Biologica (CRAB) (2004) ‘Gli antichi mais del Piemonte.’ (Graffio Press: Borgone di Susa, TO, Italy) Available at http://www.antichimaispiemontesi.it/files/mais-piemontesi.pdf
Clements MJ, Kleinschmidt CE, Maragos CM, Pataky JK, White DG (2003) Evaluation of inoculation techniques for Fusarium ear rot and fumonisin contamination of corn. Plant Disease 87, 147-153.
| Crossref | Google Scholar | PubMed |
Cömertpay G, Baloch FS, Kilian B, Ülger AC, Özkan H (2012) Diversity assessment of Turkish maize landraces based on fluorescent labelled SSR markers. Plant Molecular Biology Reporter 30, 261-274.
| Crossref | Google Scholar |
Czembor E, Waskiewicz A, Piechota U, Puchta M, Czembor JH, Stepień Ł (2019) Differences in ear rot resistance and Fusarium verticillioides-produced fumonisin contamination between Polish currently and historically used maize inbred lines. Frontiers in Microbiology 10, 449.
| Crossref | Google Scholar | PubMed |
de Mendiburu F (2017) Agricolae: statistical procedures for agricultural research. R package version 1.2.8. Available at https://cran.r-project.org/web/packages/agricolae/index.html
Devi HN, Devi KN, Singh NB, Singh TR, Jyotsna N, Paul A (2013) Phenotypic characterization, genetic variability and correlation studies among maize landraces of Manipur. International Journal of Bio-resource and Stress Management 4, 352-355.
| Google Scholar |
Djemel A, Revilla P, Hanifi-Mekliche L, Malvar RA, Álvarez A, Khelifi L (2012) Maize (Zea mays L.) from the Saharan oasis: adaptation to temperate areas and agronomic performance. Genetic Resources and Crop Evolution 59, 1493-1504.
| Crossref | Google Scholar |
Edmondson RN (2019) blocksdesign: nested and crossed block designs for factorial, fractional factorial and unstructured treatment sets. R package version 3.4. Available at https://CRAN.R-project.org/package=blocksdesign
Eschholz TW, Stamp P, Peter R, Leipner J, Hund A (2010) Genetic structure and history of Swiss maize (Zea mays L. ssp. mays) landraces. Genetic Resources and Crop Evolution 57, 71-84.
| Crossref | Google Scholar |
Gaikpa DS, Miedaner T (2019) Genomics-assisted breeding for ear rot resistances and reduced mycotoxin contamination in maize: methods, advances and prospects. Theoretical and Applied Genetics 132, 2721-2739.
| Crossref | Google Scholar | PubMed |
Gaikpa DS, Kessel B, Presterl T, Ouzunova M, Galiano-Carneiro AL, Mayer M, Melchinger AE, Schön C-C, Miedaner T (2021) Exploiting genetic diversity in two European maize landraces for improving Gibberella ear rot resistance using genomic tools. Theoretical and Applied Genetics 134, 793-805.
| Crossref | Google Scholar | PubMed |
Gerke JP, Edwards JW, Guill KE, Ross-Ibarra J, McMullen MD (2015) The genomic impacts of drift and selection for hybrid performance in maize. Genetics 201, 1201-1211.
| Crossref | Google Scholar | PubMed |
Giupponi L, Pedrali D, Leoni V, Rodari A, Giorgi A (2021) The analysis of Italian plant agrobiodiversity databases reveals that hilly and sub-mountain areas are hotspots of herbaceous landraces. Diversity 13, 70.
| Crossref | Google Scholar |
Guche MD, Pilati S, Trenti F, Dalla Costa L, Giorni P, Guella G, Marocco A, Lanubile A (2022) Functional study of lipoxygenase-mediated resistance against Fusarium verticillioides and Aspergillus flavus infection in maize. International Journal of Molecular Sciences 23, 10894.
| Crossref | Google Scholar | PubMed |
Hartings H, Berardo N, Mazzinelli GF, Valoti P, Verderio A, Motto M (2008) Assessment of genetic diversity and relationships among maize (Zea mays L.) Italian landraces by morphological traits and AFLP profiling. Theoretical and Applied Genetics 117, 831-842.
| Crossref | Google Scholar | PubMed |
Hung H-Y, Holland JB (2012) Diallel analysis of resistance to Fusarium ear rot and fumonisin contamination in maize. Crop Science 52, 2173-2181.
| Crossref | Google Scholar |
Ignjatovic-Micic D, Drinic SM, Nikolic A, Lazic-Jancic V (2008) SSR analysis for genetic structure and diversity determination of maize local populations from former Yugoslavia territories. Genetika 44, 1517-1524.
| Google Scholar | PubMed |
Ju M, Zhou Z, Mu C, Zhang X, Gao J, Liang Y, Chen J, Wu Y, Li X, Wang S, Wen J, Yang L, Wu J (2017) Dissecting the genetic architecture of Fusarium verticillioides seed rot resistance in maize by combining QTL mapping and genome-wide association analysis. Scientific Reports 7, 46446.
| Crossref | Google Scholar | PubMed |
Lanubile A, Pasini L, Lo Pinto M, Battilani P, Prandini A, Marocco A (2011) Evaluation of broad spectrum sources of resistance to Fusarium verticillioides and advanced maize breeding lines. World Mycotoxin Journal 4, 43-51.
| Crossref | Google Scholar |
Lanubile A, Logrieco A, Battilani P, Proctor RH, Marocco A (2013) Transcriptional changes in developing maize kernels in response to fumonisin-producing and nonproducing strains of Fusarium verticillioides. Plant Science 210, 183-192.
| Crossref | Google Scholar | PubMed |
Lanubile A, Maschietto V, Borrelli VM, Stagnati L, Logrieco AF, Marocco A (2017) Molecular basis of resistance to Fusarium ear rot in maize. Frontiers in Plant Science 8, 1774.
| Crossref | Google Scholar | PubMed |
Lanubile A, Giorni P, Bertuzzi T, Marocco A, Battilani P (2021) Fusarium verticillioides and Aspergillus flavus co-occurrence influences plant and fungal transcriptional profiles in maize kernels and in vitro. Toxins 13, 680.
| Crossref | Google Scholar | PubMed |
Logrieco A, Battilani P, Leggieri MC, Jiang Y, Haesaert G, Lanubile A, Mahuku G, Mesterhazy A, Ortega-Beltran A, Pasti M, Smeu I, Torres A, Xu J, Munkvold G (2021) Perspectives on global mycotoxin issues and management from the MycoKey Maize Working Group. Plant Disease 105, 525-537.
| Crossref | Google Scholar | PubMed |
Lucchin M, Barcaccia G, Parrini P (2003) Characterization of a flint maize (Zea mays L. convar. mays) Italian landrace: I. Morphophenological and agronomic traits. Genetic Resources and Crop Evolution 50, 315-327.
| Crossref | Google Scholar |
Mangiafico S (2018) rcompanion: functions to support extension education program evaluation. R package version 1.11.3. Available at https://CRAN.R-project.org/package=rcompanion
Maschietto V, Colombi C, Pirona R, Pea G, Strozzi F, Marocco A, Rossini L, Lanubile A (2017) QTL mapping and candidate genes for resistance to Fusarium ear rot and fumonisin contamination in maize. BMC Plant Biology 17, 20.
| Crossref | Google Scholar | PubMed |
Mesterházy Á, Lemmens M, Reid LM (2012) Breeding for resistance to ear rots caused by Fusarium spp. in maize – a review. Plant Breeding 131, 1-19.
| Crossref | Google Scholar |
Morales L, Marino TP, Wenndt AJ, Fouts JQ, Holland JB, Nelson RJ (2018) Dissecting symptomatology and fumonisin contamination produced by Fusarium verticillioides in maize ears. Phytopathology 108, 1475-1485.
| Crossref | Google Scholar | PubMed |
Nass LL, Paterniani E (2000) Pre-breeding: a link between genetic resources and maize breeding. Scientia Agricola 57, 581-587.
| Crossref | Google Scholar |
Oppong A, Bedoya CA, Ewool MB, Asante MD, Thompson R, Adu-Dapaah H, Lamptey JNL, Ofori K, Offei SK, Warburton ML (2014) Bulk genetic characterization of Ghanaian maize landraces using microsatellite markers. Maydica 59, 1-8.
| Google Scholar |
Ouko A, Okoth S, Netshifhefhe NEL, Viljoen A, Rose LJ (2020) Tolerance to Fusarium verticillioides infection and fumonisin accumulation in maize F1 hybrids and subsequent F2 populations. Agronomy Journal 112, 2432-2444.
| Crossref | Google Scholar |
Palumbo F, Galla G, Martínez-Bello L, Barcaccia G (2017) Venetian local corn (Zea mays L.) germplasm: disclosing the genetic anatomy of old landraces suited for typical cornmeal mush production. Diversity 9, 32.
| Crossref | Google Scholar |
Peterson BG, Carl P (2018) PerformanceAnalytics: econometric tools for performance and risk analysis. R package version 1.5.2. Available at https://CRAN.Rproject.org/package=PerformanceAnalytics
Presello DA, Reid LM, Mather DE (2004) Resistance of Argentine maize germplasm to Gibberella and Fusarium ear rots. Maydica 49, 73-81.
| Google Scholar |
Qi-Lun Y, Ping F, Ke-Cheng K, Guang-Tang P (2008) Genetic diversity based on SSR markers in maize (Zea mays L.) landraces from Wuling mountain region in China. Journal of Genetics 87, 287-291.
| Crossref | Google Scholar | PubMed |
R Core Team (2017) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org/
Reid LM, Zhu X, Parker A, Yan W (2009) Increased resistance to Ustilago zeae and Fusarium verticilliodes in maize inbred lines bred for Fusarium graminearum resistance. Euphytica 165, 567-578.
| Crossref | Google Scholar |
Robertson LA, Kleinschmidt CE, White DG, Payne GA, Maragos CM, Holland JB (2006) Heritabilities and correlations of Fusarium ear rot resistance and fumonisin contamination resistance in two maize populations. Crop Science 46, 353-361.
| Crossref | Google Scholar |
Ruiz de Galarreta JI, Alvarez A (2001) Morphological classification of maize landraces from northern Spain. Genetic Resources and Crop Evolution 48, 391-400.
| Crossref | Google Scholar |
Santiago R, Cao A, Butrón A (2015) Genetic factors involved in fumonisin accumulation in maize kernels and their implications in maize agronomic management and breeding. Toxins 7, 3267-3296.
| Crossref | Google Scholar | PubMed |
Septiani P, Lanubile A, Stagnati L, Busconi M, Nelissen H, Pè ME, Dell’Acqua M, Marocco A (2019) Unravelling the genetic basis of Fusarium seedling rot resistance in the MAGIC maize population: novel targets for breeding. Scientific Reports 9, 5665.
| Crossref | Google Scholar | PubMed |
Stagnati L, Lanubile A, Samayoa LF, Bragalanti M, Giorni P, Busconi M, Holland JB, Marocco A (2019) A genome wide association study reveals markers and genes associated with resistance to Fusarium verticillioides infection of seedlings in a maize diversity panel. G3 Genes|Genomes|Genetics 9, 571-579.
| Crossref | Google Scholar | PubMed |
Stagnati L, Rahjoo V, Samayoa LF, Holland JB, Borrelli VMG, Busconi M, Lanubile A, Marocco A (2020a) A genome-wide association study to understand the effect of Fusarium verticillioides infection on seedlings of a maize diversity panel. G3 Genes|Genomes|Genetics 10, 1685-1696.
| Crossref | Google Scholar | PubMed |
Stagnati L, Martino M, Battilani P, Busconi M, Lanubile A, Marocco A (2020b) Development of early maturity maize hybrids for resistance to Fusarium and Aspergillus ear rots and their associated mycotoxins. World Mycotoxin Journal 13, 459-471.
| Crossref | Google Scholar |
Stagnati L, Martino M, Soffritti G, Lanubile A, Ravasio A, Marocco A, Rossi G, Busconi M (2021) Microsatellite and morphological characterization of three Rostrato di Val Chiavenna (Sondrio, Italy) maize (Zea mays L.) accessions. Genetic Resources and Crop Evolution 68, 3025-3038.
| Crossref | Google Scholar |
Stagnati L, Soffritti G, Desiderio F, Lanubile A, Zambianchi S, Marocco A, Rossi G, Busconi M (2022) The rediscovery of traditional maize agrobiodiversity: a study case from northern Italy. Sustainability 14, 12110.
| Crossref | Google Scholar |
Torri A, Lanzanova C, Locatelli S, Valoti P, Balconi C (2015) Screening of local Italian maize varieties for resistance to Fusarium verticillioides. Maydica 60, 1-8.
| Google Scholar |
Verderio A, Bosio M, Introzzi F, Livini C, Motto M (1989) Relazioni tra prolungata persistenza fogliare e componenti della produzione in ibridi di mais (Zea mays L.). Agronomia 23, 173-177.
| Google Scholar |
Zila CT, Samayoa LF, Santiago R, Butrón A, Holland JB (2013) A genome-wide association study reveals genes associated with Fusarium ear rot resistance in a maize core diversity panel. G3 Genes|Genomes|Genetics 3, 2095-2104.
| Crossref | Google Scholar | PubMed |
Zila CT, Ogut F, Romay MC, Gardner CA, Buckler ES, Holland JB (2014) Genome-wide association study of Fusarium ear rot disease in the U.S.A. maize inbred line collection. BMC Plant Biology 14, 372.
| Crossref | Google Scholar | PubMed |