Revista Mexicana Ciencias Agrícolas   volume 11   number 2   February 15 - March 31, 2020

DOI: https://doi.org/10.29312/remexca.v11i2.1874

Essay

Resistance to Fusarium causing rots in wheat: topicality
and prospects for its use in Mexico

María del Pilar Suaste-Franco1

Gabriel Iturriaga-de la Fuente1

Ernesto Solís-Moya2

Juan Carlos Raya-Pérez1

Juan Gabriel Ramírez-Pimentel1

Luis Antonio Mariscal-Amaro2§

1National Technology of Mexico-Roque Technological Institute (TecNM-IT Roque). Celaya-Juventino Rosas Highway km 8, Celaya, Guanajuato, Mexico. CP. 38110. (suastef.mp@hotmail.com; gaiturriaga@itroque.edu.mx; juancarlos.raya@gmail.com; garamirez@itroque.edu.mx). 2Wheat and Oat and Forest and Agricultural Health Programs-Bajío Experimental Field-INIFAP. Celaya-San Miguel de Allende Highway km 6.5, Celaya, Guanajuato, Mexico. CP. 38110. (solis.ernesto@inifap.gob.mx).

§Corresponding author: mariscal.luis@inifap.gob.mx.

Abstract

Root rot, crown and stem rot in wheat are considered a serious threat to this cereal in various parts of the world since the losses that cause grain yield and quality reach up to 89% and can be comparable to those caused by rust, in addition to the fungi associated with these rotting synthesize mycotoxins that can contaminate food products. This problem in Mexico has been little studied; however, in recent years, these diseases in irrigation and temporary wheats have been more incidents which is causing concern in the producers of this cereal in the country. This review summarizes current aspects of the disease, the sources of resistance available worldwide, as well as how this resistance operates in the Fusarium-wheat patosystem. The genetic basis of resistance to root, stem and crown rot of hexaploid wheats has been examined; through the mapping of Quantitative Trait Loci (QTL). To date, 44 QTL have been identified on 14 chromosomes with alleles that induce resistance to this disease and that are derived from hexaploid wheats and close relatives. Genetic improvement for this disease through introgression of alleles with these QTL is the most feasible strategy and the pyramidation of these QTL seems to be the most viable strategy in genetic improvement programs. Important step for the management of the problem in the wheat producing areas in Mexico

Keywords: Triticum aestivum L., genetics, QTL, wilting.

Reception date: January 2020

Acceptance date: February 2020

Globally, wheat cultivation is affected by different microorganisms that decrease their yield, of these, the fungi of the genus Puccinia that cause different rusts are considered the most harmful; however, another group of fungi causing root, stem and crown rot (PRC) belonging to a complex of the genus Fusarium (Mariscal et al., 2018) has been identified for soil pathogens in this cereal.

In the field, PRC can cause brown lesions in seedlings that appear in the root, crown, in the leaf sheaths and in the lower stem and in adult stage, a copper wilt of the spikes of the diseased plants is observed, different from the hue white caused by spike gnaw or the usual golden bream of healthy ripe spikes (Mariscal et al., 2018). This problem has a greater impact when there is a period of water stress during the development of the seedling and after the anthesis until maturity (Moya, 2013; Liu et al., 2015).

The importance of these fungi, in addition to the yield losses they cause and can reach up to 89% (in monetary value, losses of up to 68 million dollars) (Klein et al., 1991; Smiley et al., 2005; Liu et al., 2015), is that, due to their biology, they can develop persistent survival structures (clamidospores) that can remain viable in the soil for several years.

They can synthesize mycotoxins: zearalenone, nivalenol, deoxinivalenol, 3-acetyldeoxynivalenol, 15-acetyldeoxynivalenol, diacetoxyscirpenol, neosolaniol, fusarenone X and fumonisins that contaminate the grain and other tissues (Ferreira et al., 2006; Mudge et al., 2006; Pinto et al., 2008; Orantes et al., 2011; Martínez et al., 2014; Rebib et al., 2014) and may even contaminate food products such as flour and buckwheat (Bertecheni et al., 2012).

Different species of Fusarium that cause PRC have been identified. Globally, the most frequent species and with which the majority of genetic studies have been done are: F. graminearum and F. pseudograminearum (Kazan and Gardiner, 2018), but F. culmorum has also been identified (Scherm et al., 2013), F. avenaceum, F. acuminatum, F. crookwellense, F. poae (Cook, 2010), F. equiseti, F. hostae and F. redolens (Shikur et al., 2018) causing such diseases. In Mexico, in irrigation and temporary wheat, the species F. proliferatum, F. poae, F. verticillioides, F. subglutinans, F. oxysporum, F. thapsinum, F. andiyazi, F. graminearum, F. avenaceum, F. equiseti and Microdochium nivale (Gilchrist et al., 2005; Limón et al., 2016; Leyva et al., 2017; Rangel et al., 2017). PRC in wheat can occur in all the producing areas of this cereal and are considered more aggressive in humid climates (Gilchrist et al., 2005).

In areas where the humidity is low, the infection is almost exclusively caused by the inoculum present in crop residues (Gilchrist et al., 2005). It has been observed that the incidence of the different species of the genus Fusarium associated with PRC varies year by year and depends largely on the climatic conditions and geography of the wheat regions, with some species being more frequent in low humidity regions relative low while others affect more in high regions with moderate to high relative humidity (Gilchrist et al., 2005).

This indicates their high level of adaptation as members of a complex of pathogens that respond to changes in temperature, humidity and edaphic factors (Moya, 2013). It is also mentioned that warm temperatures in the months of February, March, April and May, as well as early sowing, water stress, soil with high temperatures, soil cracking induced by rains, and even the lack of microelements such as Zinc (usable by the plant) in the soil, lead to a higher incidence of the disease (Singh et al., 1996; Smiley et al., 2005; Saremi et al., 2007; Khoshgoftarmanesh et al., 2010; Poole et al., 2013).

Several authors report that sowing under minimum or conservation tillage, rotation schemes (mainly with corn and barley) and the increase in the dose of nitrogen are the main agronomic factors that increase the incidence of Fusarium species that cause PRC (Lamprecht et al., 2006; Chakraborty et al., 2006; Liu et al., 2015; Limón et al., 2016; Chekali et al., 2016; Zheng et al., 2017). It has been observed that plants with excess of N deplete the water supply of the soil more quickly so that they suffer from premature water stress which leads to a higher incidence of the disease (Davis et al., 2009).

On the other hand, several species of this genus of fungi, which cause leaf spots and blight on the spike and rot on the spike (stem of the spike), remain as contaminants of the same grain that serves as a source of primary inoculum from where the PRC from seedling (Stenglein et al., 2012). According to several authors, control strategies that decrease the incidence of Fusarium species that cause PRC in wheat include: 1) crop rotation with crucifers or legumes that help break the fungus's biological cycle (Lamprecht et al., 2006; Chekali et al., 2016); and 2) threshing at optimal dates that allows less grain contamination; 3) adequate and fractional fertilization that avoids the application of excessive doses of N; 4) the incorporation of zinc in soils lacking this element; 5) crop waste management; 6) Seed treatment with fungicides; and 7) the use of varieties resistant to disease, with tolerance to water stress, or efficient in the use of zinc (Sing  h et al., 1996; Burgess et al., 2001; Edwards, 2004; Burgess, 2005; Lozano et al., 2006; Davis et al., 2009; Khoshgoftarmanesh et al., 2010; Zheng et al., 2017).

Globally and in Mexico, the genetic improvement of wheat for resistance or tolerance to this disease should be a constant activity, as well as the identification of sources of resistance and studies that allow understanding the genetic basis of resistance to PRC in this cereal. This review aimed to summarize the advances of genetic improvement for PRC, as well as the genetic basis of resistance to this disease in flour wheats.

Root and stem rot resistance components

The genetics of PRC resistance has been reported in some wheat genotypes and the available results suggest that this resistance, as well as the resistance to spike rust (RE) caused by F. graminearum or F. pseudograminearum, is also of a polygenic nature, of minor or quantitative genes; although, due to the magnitude of the reduction in the severity of crown rot that may be conferred by a single QTL, some authors suggest that this resistance may be due to larger genes (Ma et al., 2010).

The common etiology between RE and PRC raises the possibility that resistance to these two diseases is given by the same genes (Bing et al., 2010). However, these authors when evaluating the same wheat genotypes for both resistance to RE and PRC, found that the QTL associated with both resistances are found on different chromosomes.

Similarly, it has been reported that QTL associated exclusively with resistance to PRC are also found in different chromosomes. The above suggests that the genetic mechanism for PRC resistance is multigenetic and different from that of RE resistance (Ma et al., 2010; Bing et al., 2010). Ma et al. (2014) mention that the `Sumai 3ʼ genotype, the source of the best resistance known for RE, has a QTL on the short arm of chromosome 3B, considered as a major locus that provides resistance to this disease.

The 3BS locus contains a glycosyltransferase gene with the potential to detoxify mycotoxin deoxinivalenol which is a virulence factor; however, the QTL 3BS does not confer any significant level of resistance to PRC (Ma et al., 2014). In another study Ma et al. (2010) confronted the species F. graminearum and F. pseudograminearum against a population of plants of the cross between ʻCSCR6ʼ/ʻLangʼ. With these two species, the same two QTL were detected in the population, which suggested that resistance to PRC in wheat is not specific to the species of the fungus.

It is important to mention that in resistance studies with hard wheats it has been observed that tetraploid wheats are more susceptible to PRC than hexaploids (Ma et al., 2012). It has also been observed that resistance to this disease may be influenced by morphological characteristics of the plant since Liu et al. (2010) when studying the relationship between plant height and crown rot, they found that dwarf wheat lines were more resistant to crown rot than high lines, due to physiological and structural characteristics such as cell density in the dwarf lines.

Genetic sources for wheat resistance improvement

In countries such as the United States of America, Australia, India and Canada, PRC have been a problem known for several years, so efforts to find sources of resistance have been greater. Different authors have evaluated, in common, some hexaploid wheat genotypes confronted against F. pseudograminearum, observing that some materials such as ʻ2-49ʼ, ʻIRN497ʼ and ʻSuncoʼ.

They have been the most tolerant to PRC with percentages of disease severity ranging from 4.2-32% in seedlings and 24-67.1% in adult plants (Bovill et al., 2010; Martin et al., 2015). Bing et al. (2010) when evaluating 32 wheat genotypes confronted against F. graminearum and F. pseudograminearum, they observed that the seedling genotypes that were more tolerant to these two species in the greenhouse were ʻ2-49ʼ, ʻAbura komugiʼ, ʻAso zairaiʼ, ʻAso zairai 11ʼ, ʻChileʼ and ʻErnieʼ with values on the visual scale used from 0= no symptoms to 1= obvious necrotic lesions in the beetle or in the sheath of the first leaf.

The tolerance of flour wheat materials has also been evaluated based on the percentage of withered spikes, reflecting root damage, and in this case, the materials that were classified as tolerant, to these two fungi, with <20% spikes in this condition were ʻ2-49ʼ, ʻL2-120ʼ, ʻFrontanaʼ, ʻJanzʼ, ‘Langʼ, ʻEGA Wileyʼ, ‘Magentaʼ, ʻDrysdaleʼ, ʻHartogʼ, ʻWyalkatchemʼ and ʻE34ʼ (Klein et al., 1985; Wildermuth and McNamara, 1994; Li et al., 2008). Ma et al. (2010) when evaluating different wheat genotypes confronted against F. graminearum and F. pseudograminearum found that the ʻCSCR6ʼ genotype was the most tolerant of the disease.

In another similar study, et al. (2006), when evaluating different wheat genotypes in a greenhouse trial, against these two species of the fungus, determined that the genotypes ʻSuncoʼ, ʻLangʼ, ʻ22397ʼ, ʻRowanʼ, ʻSunstateʼ, ʻBaxerʼ, ʻSunbriʼ and ʻSunvaleʼ were the ones with the lowest severity index of the illness. Wildermuth et al. (2001); Wallwork et al. (2004) evaluated different lines of flour wheats, synthetic wheats and hard wheats confronted against F. pseudograminearum.

According to these authors, the most tolerant genotypes in adult plants were the flour wheats ʻ2-49ʼ, ʻGluyas Earlyʼ, ʻKukriʼ and ʻSuncoʼ, the synthetic wheats ʻCIMMYT elite synthetic 62ʼ, ʻCIMMYT elite synthetic 97ʼ, ʻCIMMYT scab synthetic 92ʼ, ʻCIMMYT scab synthetic , ʻCIMMYT scab synthetic 101ʼ and ʻCIMMYT scab synthetic 104ʼ and wheats ʻAUS 11434ʼ (T. dicoccum), ʻAUS 18694ʼ (T. zhukovskyi), ʻAUS 18743ʼ (T. dicoccum) and ʻT96-5317ʼ (T. dicoccum), all these lines presented a severity of the disease from 0% to 50%.

When assessing necrosis due to greenhouse seedlings, Leyva et al. (2017) used the combination of F. proliferatum and F. graminearum against different wheat genotypes, observing the Mexican varieties Galvez M87ʼ, ʻCastrejon F97ʼ, ʻTlaxcala F2000ʼ, `Salamanca S86ʼ and ʻMaya S2007ʼ as tolerant. Ma et al. (2010) evaluated a backcross between the parents `Belloriʼ/ʻCSCR6ʼ, the first a durum wheat (Triticum durum) highly susceptible to PRC and the second a genotype of the disease-resistant T. spelta species, obtained a population they confronted against F. pseudograminearum. These authors observed that some segments of a large section of chromosome 6B of the donor resistant parent significantly increased resistance to PRC in durum wheat.

QTL mapping for resistance to root and crown rot in wheat

Table 1 shows the list of significant QTL identified in hexaploid wheats and close relatives in different studies worldwide. Wheat materials are presented where the QTL were identified, the denomination of the QTL (although in many cases these are mentioned without denomination), the chromosome where they were identified, either in their long arm (L) or short arm (S), the or markers used for identification, phenotypic variance in percentage contributed by each QTL, the species of the fungus used in the study, the evaluated character, the stage of the plant where the resistance given by the QTL was observed and the references.

Table 1. List of QTL that confer resistance to root, crown and stem rot in wheat.

GEN= genotype; QTL= QTL denomination; SD= no denomination; LOC= chromosome where it is located; MA= markers and/or interval; VF%= phenotypic variation in percentage; EH= fungus used; Fp= Fusarium pseudograminearum; Fc= F. culmorum; Fg= F. graminearum; CA= character evaluated; SE= severity of the disease; ES= symptom extension; EN= extent of necrosis; PL= seedling; PA= adult plant; REF= reference.

Resistance genes associated with root and crown rot

Ma et al. (2014) when studying and identifying linked genes and transcriptional changes of the QTL called Qcrs-3B, of the 3BL chromosome, in isogenic wheat lines, observed the induction of 1809 genes after inoculation of seedlings with F. pseudograminearum. 638 highly regulated genes contained 46 pathogen-related coding proteins, 42 encoding kinase-like receptors, 21 encoding P450 cytochromes, 17 encoding glutathione transferase and 10 encoding detoxification-related proteins.

These genes also contained proteins involved in the pathogen-host interaction: 14 for proteins related to disease resistance, 6 for proteins related to cell wall, 4 for WIR1 proteins (wheat-induced type 1 resistance), 7 for factors of WRKY transcription, 3 for ascorbate peroxidases; 6 for phenylalanine-ammonium liases and 14 for germin-like proteins (GLP).

As well as, genes for the biosynthesis of phytohormones involved in the wheat-Fusarium interaction: jasmonic acid, ethylene and salicylic acid. On the other hand, 22 low regulation genes studied were related to the encoding of RGA1 resistance proteins, calcium-bound proteins with the EF-hand domain and a senescence-associated protein (Ma et al., 2014). Motallebi et al. (2015) after inoculating plants of the resistant genotype ʻSumai3ʼ with F. culmorum.

They observed the synthesis of defense-related enzymes: superoxide dismutase (SOD), catalase (CAT), peroxidases (POX), polyphenol oxidase (PPO), lipoxygenase (LOX) and phenylalanine ammonium lyase (PAL). Zheng et al. (2015) when mapping the QTL Qcrs.cpi-3B in nearby isogenic wheat lines, they found that in the locus interval where this QTL was found, genes encoding different disease resistance proteins were identified as rga2, rpm1, rga4, of synthesis of metallothionein, NBS-LRR of partial resistance, and those such as proteins 2 and 3 similar to rpp13, similar to those of the AP3 complex of the beta-A subunit and similar to those of gibberellin-2-beta-dioxygenase 8.

Desmond et al. (2006) studied the expression of 26 wheat genes related to resistance to F. pseudograminearum. The expression of these genes was evaluated in the susceptible genotype ʻKennedyʼ and in the partially resistant genotype ʻSuncoʼ. The induction of eight defense genes was observed: PR1.1, PR2 (β, 1-3 glucanase), PR3 (chitinase), PR4 ‘wheatwin’ - ribonuclease activity), PR5 (thaumatine-like protein), TaPERO ( peroxidase), PR10 and TaGLP2a (germin-like protein).

The TaPERO gene encodes a peroxidase enzyme that has frequently been implicated in cell wall modifications and in the metabolism of reactive oxygen species. The TaGLP2a gene encodes a protein with superoxide dismutase activity. The PR1, PR2, PR3, PR4 and PR5 genes encode homologs of plant PR proteins. Wang et al. (2018) when evaluating wheat materials `Florence-Auroreʼ (resistant), ʻSumai 3ʼ (susceptible), ʻFrontanaʼ (susceptible) and ʻNing 7840ʼ (highly susceptible) against F. graminearum observed the expression of the genes TaUGT12887, TaUGT3, CYP709C1, WZF1, WFhb1-c1 and TaMDR1 in root tissue cells from day 1 to 21 after inoculation.

These genes are mainly associated with the ability of the plant to detoxify DON mycotoxins, the trichothecene family and jasmonate signaling. Earlier, it is mentioned that wheat plants show more severe symptoms of PRC under water stress, both in greenhouse and field studies. One of the possible reasons for the interaction between drought and resistance to PRC, is that drought can affect some morphological characteristics of the plant such as height and days to spike.

Characters that have been reported to have a strong influence on PRC resistance in wheat and barley. Another possibility is that the same genes could be associated in both drought tolerance and resistance to PRC. In this regard, Ma et al. (2015) studying malondialdehyde, a product of lipid peroxidation, frequently used as a parameter to assess the cellular damage of plants due to water stress, mapped the QTL called Qheb.mda-3B on chromosome 3B. This QTL controls the malondialdehyde content in both plants with and without water stress.

The QTL Qheb.mda-3B was located in the same genetic range as the QTL Qcrs.cpi-3B that controls the resistance to PRC. The results of these authors again suggest that the same set of genes is probably involved in both drought tolerance and resistance to PRC.

Strength improvement for root and crown rot in wheat

Genetic pyramidation has been used as an effective approach that allows multiple and durable resistance to be achieved, and has been effective for resistance to PRC in barley, rice scalding, sunflower mildew and yellow linear rust in wheat (Chen et al., 2015; Zheng et al., 2017). Zheng et al. (2017) evaluated the QTLs called Qcrs.cpi-3B, Qcrs.cpi-5D and Qcrs.cpi-2D, of two

segregating populations from the PRC resistant progenitors, ʻCSCR6ʼ (accession of Triticum spelta) with locus 3BL, ʻEGA Wylieʼ (Australian commercial variety) with the two 5DS and 2DL loci and the Australian and Chinese susceptible commercial varieties ʻLangʼ and ʻSumai3ʼ, respectively.

Both populations clashed against F. pseudograminearum. The results of this study showed a significant variation in the values of the disease index (IE) in the lines with the same alleles of the QTL evaluated. Comparing with the lines without any resistant allele, those with a resistance allele reduced the IE values between 21 and 33%. Lines with a combination of two resistance alleles reduced IE values between 36 and 38% and lines with all three alleles reduced IE values, 60% on average.

Bovill et al. (2010) compared the resistance levels of individuals with different combinations of QTL from each of the donor parents. In the ʻ2-49ʼ/ʻW21MMT70ʼ population, the lines with the presence of the three QTL, QCr.usq-1D.1, QCr.usq-3B.1 and one with no denomination located on chromosome 7A, were significantly more resistant to PRC than those without any QTL. The lines with the combination QCr.usq-1D.1 and QCr.usq-3B.1 showed a reduction in the severity of the crown rot of 51.2%, compared to those without any QTL.

The lines without the two QTL mentioned above, but with the QTL of chromosome 7A, showed a severity of 15% lower than those lines without any of them. In the ʻ2-49ʼ/ʻSuncoʼ population it was observed that the lines with three QTL were significantly more resistant to crown rot with 28% less severity than those without any resistance allele. Bovill et al. (2006) identified three QTL located on chromosomes 2D, 5D and 2B, the first two inherited from the hexaploid wheat line ʻW21MMT70ʼ and the third inherited from ʻMendosʼ.

A population of 95 double haploid lines from the cross between these two parents was evaluated. The population was confronted against F. pseudograminearum. The results of this study showed that those lines with only one of the three alleles showed percentages of disease severity >50 <60%, the lines with the combination of two alleles had percentages of the disease >45 <50%, and those with the three alleles they presented percentages of >40 <45%. The lines without any allele presented percentages of the average disease of 97.6%.

Conclusions

Root, crown and stem rot in wheat flour is a serious problem worldwide. In Mexico this problem, called the wheat dryer or fusariosis, has been increasingly incident and the losses it causes could be compared to those caused by rust. Given this scenario, it is urgent that genetic improvement programs develop a greater number of varieties resistant to this disease.

For this, the constant evaluation of advanced varieties and lines of wheat is necessary for their resistance or tolerance to the disease to have a range of materials that can be used as parents for future crossing plans along with genetic pyramidation. Several QTLs have been detected in wheat materials from different parts of the world, but the identification of resistance QTL in wheat materials adapted to the different wheat regions of the country has been null, so it is necessary to start with this type of study.

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