Beet necrotic yellow vein virus genome reassortments in a resistant sugar beet variety showing–in a small area in France–strong rhizomania symptoms

Koenig, R.; Holtschulte, B.; Deml, G.; Lüddecke, P.; Schuhmann, S.; Maaß, Christina; Richert-Pöggeler, Katja

doi:10.1007/bf03356279

Cited by 8 publications

(11 citation statements)

References 13 publications

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“…As RNA5-containing strains were identified long before the large-scale cultivation of Rz1 genotypes, an evolutionary interrelation or selection by Rz1 has never been speculated. Moreover, these strains do not spread rapidly, but mix with types A and B at the border of infected areas, suggesting the reassortment of both strain types (Koenig et al, 2009a). The occurrence of the more widely distributed strains carrying four RNA components with RB properties in different geographical regions has been associated with specific P25 tetrad compositions: VCHG, VLHG and AYPR (Liu and Lewellen, 2007;Liu et al, 2005;Pferdmenges et al, 2008;Bornemann et al, unpublished results).…”

Section: Introductionmentioning

confidence: 98%

Effect of sugar beet genotype on the Beet necrotic yellow vein virus P25 pathogenicity factor and evidence for a fitness penalty in resistance‐breaking strains

Bornemann¹,

Varrelmann²

2013

Molecular Plant Pathology

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Beet necrotic yellow vein virus (BNYVV), vectored by Polymyxa betae, causes rhizomania in sugar beet. For disease control, the cultivation of hybrids carrying Rz1 resistance is crucial, but is compromised by resistance-breaking (RB) strains with specific mutations in the P25 protein at amino acids 67-70 (tetrad). To obtain evidence for P25 variability from soil-borne populations, where the virus persists for decades, populations with wild-type (WT) and RB properties were analysed by P25 deep sequencing. The level of P25 variation in the populations analysed did not correlate with RB properties. Remarkably, one WT population contained P25 with RB mutations at a frequency of 11%. To demonstrate selection by Rz1 and the influence of RB mutations on relative fitness, competition experiments between strains were performed. Following a mixture of strains with four RNAs, a shift in tetrad variants was observed, suggesting that strains did not mix or transreplicate. The plant genotype exerted a clear influence on the frequency of RB tetrads. In Rz1 plants, the RB variants outcompeted the WT variants, and mostly vice versa in susceptible plants, demonstrating a relative fitness penalty of RB mutations. The strong genotype effect supports the hypothesized Rz1 RB strain selection with four RNAs, suggesting that a certain tetrad needs to become dominant in a population to influence its properties. Tetrad selection was not observed when an RB strain, with an additional P26 protein encoded by a fifth RNA, competed with a WT strain, supporting its role as a second BNYVV pathogenicity factor and suggesting the reassortment of both types.

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Section: Introductionmentioning

confidence: 98%

Effect of sugar beet genotype on the Beet necrotic yellow vein virus P25 pathogenicity factor and evidence for a fitness penalty in resistance‐breaking strains

Bornemann¹,

Varrelmann²

2013

Molecular Plant Pathology

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“…This suggests that Rz1 resistance-breaking by the P-type might depend on RNA5 rather than on P25 tetrad mutations. Interestingly, Koenig et al (2009b) found in field root samples of Rz1 resistant plants from the Pithiviers area genome reassortments consisting of either A-/P-type or B-/P-type. More recently, Galein et al (2018) confirmed this observation in the same area and could even identify plants containing A-, B-, and P-type.…”

Section: Introductionmentioning

confidence: 99%

Application of a Reverse Genetic System for Beet Necrotic Yellow Vein Virus to Study Rz1 Resistance Response in Sugar Beet

Liebe¹,

Wibberg

Maiß

et al. 2020

Front. Plant Sci.

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Beet necrotic yellow vein virus (BNYVV) is causal agent of rhizomania disease, which is the most devastating viral disease in sugar beet production leading to a dramatic reduction in beet yield and sugar content. The virus is transmitted by the ubiquitous distributed soil-borne plasmodiophoromycete Polymyxa betae that infects the root tissue of young sugar beet plants. Rz1 is the major resistance gene widely used in most sugar beet varieties to control BNYVV. The strong selection pressure on the virus population promoted the development of strains that can overcome Rz1 resistance. Resistance-breaking has been associated with mutations in the RNA3-encoded pathogenicity factor P25 at amino acid positions 67-70 (tetrad) as well as with the presence of an additional RNA component (RNA5). However, respective studies investigating the resistance-breaking mechanism by a reverse genetic system are rather scarce. Therefore, we studied Rz1 resistance-breaking in sugar beet using a recently developed infectious clone of BNYVV A-type. A vector free infection system for the inoculation of young sugar beet seedlings was established. This assay allowed a clear separation between a susceptible and a Rz1 resistant genotype by measuring the virus content in lateral roots at 52 dpi. However, mechanical inoculation of sugar beet leaves led to the occurrence of genotype independent local lesions, suggesting that Rz1 mediates a root specific resistance toward BNYVV that is not active in leaves. Mutation analysis demonstrated that different motifs within the P25 tetrad enable increased virus replication in roots of the resistant genotype. The resistance-breaking ability was further confirmed by the visualization of BNYVV in lateral roots and leaves using a fluorescent-labeled complementary DNA clone of RNA2. Apart from that, reassortment experiments evidenced that RNA5 enables Rz1 resistance-breaking independent of the P25 tetrad motif. Finally, we could identify a new resistance-breaking mutation, which was selected by high-throughput sequencing of a clonal virus population after one host passage in a resistant genotype. Our results demonstrate the feasibility of the reverse genetic system for resistance-breaking analysis and illustrates the genome plasticity of BNYVV allowing the virus to adapt rapidly to sugar beet resistance traits.

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“…This tetrad was linked with resistance-breaking (RB) events, i.e. with the emergence of symptoms in cultivars considered tolerant or resistant (Acosta-Leal and Rush, 2007 ; Liu and Lewellen, 2007 ; Koenig et al, 2008 , 2009a ; Acosta-Leal et al, 2010 ).…”

Section: Introductionmentioning

confidence: 99%

“…Despite the relative diversity of BNYVV strains, mixed infections have only rarely been reported (Koenig et al, 2009a ). Ratti et al ( 2006 ) detected only a single A/B type infection out of 72 European samples.…”

Section: Introductionmentioning

confidence: 99%

Long Term Management of Rhizomania Disease—Insight Into the Changes of the Beet necrotic yellow vein virus RNA-3 Observed Under Resistant and Non-resistant Sugar Beet Fields

2018

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Rhizomania disease, caused by the Beet necrotic yellow vein virus (BNYVV), is considered as one of the major constraints for sugar beet production, worldwide. As a result of the introgression of major resistance genes (Holly, Rz2) in commercially available sugar beet varieties, the virus has endured strong selection pressure since the 90s'. Understanding the virus response and diversity to sugar beet resistance is a key factor for a sustainable management of only few resistance genes. Here we report rhizomania surveys conducted in a rhizomania hot spot, the Pithiviers area (France) during a 4-year period and complementary to the study of Schirmer et al. (2005). The study aimed at evaluating the intra- and inter-field BNYVV diversity in response to different sources of resistance and over the growing season. To follow rhizomania development over the sugar beet growing season, extensive field samplings combined with field assays were performed in this study. The evolution of the BNYVV diversity was assessed at intra- and inter-field levels, with sugar beet cultivars containing different resistance genes (Rz1, Rz1 + Heterodera schachtii resistance and Rz1Rz2). Intra-field diversity was analyzed at the beginning and the end of the growing season of each field. From more than one thousand field samples, the simultaneous presence of the different A, B and P types of BNYVV was confirmed, with 21 variants identified at positions 67–70 of the p25 tetrad. The first variant, AYHR, was found most commonly followed by SYHG. Numerous mixed infections (9.93% of the samples), mostly of B-type with P-type, have also been evidenced. Different tetrads associated with the A- or B-type were also found with a fifth RNA-genome component known to allow more aggressiveness to BNYVV on sugar beet roots. Cultivars with Rz1+Rz2 resistant genes showed few root symptoms even if the BNYVV titre was quite high according to the BNYVV type present. The virus infectious potential in the soil at the end of the growing season with such cultivars was also lower despite a wider diversity at the BNYVV RNA3 sequence level. Rz1+Rz2 cultivars also exhibited a lower presence of Beet soil-borne virus (BSBV), a P. betae-transmitted Pomovirus. Cultivars with Rz1 and nematode (N) resistance genes cultivated in field infected with nematodes showed lower BNYVV titre than those with Rz1 or Rz1+Rz2 cultivars. Overall, the population structure of BNYVV in France is shown to be different from that previously evidenced in different world areas. Implications for long-term management of the resistance to rhizomania is discussed.

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Beet necrotic yellow vein virus genome reassortments in a resistant sugar beet variety showing–in a small area in France–strong rhizomania symptoms

Cited by 8 publications

References 13 publications

Effect of sugar beet genotype on the Beet necrotic yellow vein virus P25 pathogenicity factor and evidence for a fitness penalty in resistance‐breaking strains

Effect of sugar beet genotype on the Beet necrotic yellow vein virus P25 pathogenicity factor and evidence for a fitness penalty in resistance‐breaking strains

Application of a Reverse Genetic System for Beet Necrotic Yellow Vein Virus to Study Rz1 Resistance Response in Sugar Beet

Long Term Management of Rhizomania Disease—Insight Into the Changes of the Beet necrotic yellow vein virus RNA-3 Observed Under Resistant and Non-resistant Sugar Beet Fields

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