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Resistance of Iranian landrace wheat to the cereal cyst nematode, Heterodera filipjevi

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ORIGINAL PAPER

Resistance of Iranian landrace wheat to the cereal cyst nematode,

Heterodera filipjevi

Elif Yavuzaslanoglu1&I. Halil Elekcioglu2&Julie M. Nicol3&Jason G. Sheedy4

Received: 21 March 2016 / Accepted: 13 June 2016 / Published online: 16 June 2016 # Australasian Plant Pathology Society Inc. 2016

Abstract The cereal cyst nematode (CCN), Heterodera filipjevi,has a global distribution and can reduce wheat yields by up to 32 %. Plant genetic resistance can effectively manage H. filipjevi populations, so 31 Iranian wheat landrace acces-sions were screened for H. filipjevi resistance under green-house conditions. PI628144 (syn. AUS28321) was resistant and five other accessions moderately resistant to H. filipjevi and may provide novel CCN-resistance for plant breeders to exploit.

Keywords Plant breeding . Cereal cyst nematode . Heterodera filipjevi . Landrace . Resistance . Wheat

Wheat (Triticum aestivum) is the most common commodity in Turkey with about 16 Mt. produced from 7 Mha area annually (TUIK2015). Cereal cyst nematodes (CCN; Heterodera spp.) and root lesion nematodes (RLN; Pratylenchus spp.) limit this production. Heterodera filipjevi is widely distributed and has been reported in cereal crops from Europe (Cook and Noel

2002; Holgado et al. 2004), Asia (Bishnoi and Bajaj 2002; Tanha Maafi et al. 2003; Li et al.2010) and North America (Smiley et al. 2008; Dyer et al. 2015). It is also widespread in the Turkish Central and East Anatolian Regions (Yavuzaslanoglu et al. 2012; Toktay et al. 2015), where it has been shown to reduce wheat yields by up to 32 % (Nicol et al.2006). Geographical distribution of CCN in Turkey is closely related to climate. The H. filipjevi-domi-nated Central and Eastern Anatolia have a temperate climate, while the H. latipons and H. avenae-dominated South-Eastern Anatolian, Eastern Mediterranean, Aegean and Thrace re-gions (Misirlioglu and Pehlivan2007; Imren et al.2015) are warmer with a Mediterranean climate. Information on CCN pathotypes in Turkey is limited, with populations of H. filipjevi from some locations in Central and South-Eastern Anatolia similar to H. avenae pathotype Ha33 (Toktay et al. 2013) and H. avenae populations from Eastern Mediterranean and South-Eastern Anatolia identified as pathotype Ha21 (Imren et al.2013). The use of non-host crops and resistant cultivars, where available, are considered effective strategies for reducing CCN populations and keeping them below gional damage thresholds. Many of the genes conferring re-sistance to CCN are single genes with large effect and subse-quently their use risks the breakdown of resistance (Lasserre et al.1996) or in mixed nematode populations, changing the relative population densities such that other phytoparasitic species dominate (Lasserre et al. 1994). Identifying wheat accessions with novel resistance to H. filipjevi or accessions with resistance to multiple diseases will help mitigate these risks. The aim of this study was to identify potentially novel sources of resistance to H. filipjevi in a collection of 31 Iranian landraces previously evaluated for resistance to RLN (Pratylenchus thornei) (Sheedy and Thompson2009).

The 31 landraces screened in this study were provided by the International Wheat and Maize Improvement Centre

* Elif Yavuzaslanoglu elifs3@hotmail.com

1 Technical Sciences Vocational School, Department of Plant and

Animal Production, Karamanoglu Mehmetbey University, Karaman, Turkey

2

Faculty of Agriculture, Department of Plant Protection, Cukurova University, Adana, Turkey

3

International Maize and Wheat Improvement Centre (CIMMYT), Texcoco, Mexico

4 Centre for Crop Health, Institute for Agriculture and the

Environment, University of Southern Queensland (USQ), Toowoomba, QLD 4350, Australia

Australasian Plant Pathol. (2016) 45:411–414 DOI 10.1007/s13313-016-0427-2

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(CIMMYT, Mexico) and were compared with four reference wheat cultivars, namely Bezostaya and Kutluk (susceptible), Silverstar (moderately resistant) and Sönmez (Yavuzaslanoglu et al.2015).

The accessions were grown under greenhouse conditions at 25 ± 3 °C with a 16 h photoperiod. A 7 day old pre-germinated seedling was transferred to 30 mm diameter plastic tube (130 mm high; 92 mL capacity) filled with a mix of sand,

field soil and organic matter (70:29:1). The transplanted seed-ling was inoculated with 100 H. filipjevi J2 s, extracted from field soil collected near Haymana, Turkey (39°24′13″N, 32°37′14″E), and re inoculated with an additional 100 J2 s 24 h later. Six replicates were assessed for each entry and arranged in a randomised block design. Nine weeks after in-oculation, cysts were collected from both roots and soil by washing the samples through nested 850 and 250μm sieves.

Table 1 Mean number of Heterodera filipjevi cysts per plant, provisional resistance group and origin of Iranian wheat

landrace accessions (1United

States Department of Agriculture

accession number;2Australian

Grains Gene Bank accession

number;3Back-transformed mean;4R: resistant, MR: moderately resistant, MRMS: moderately resistant-moderately susceptible, MS: moderately susceptible, S: susceptible)

Accession1 Synonym2 Originof accessions

(Country, Province/State)

H. filipjevi cysts/ plant Provisional

resistance

group4

ln(x + 1) BTM3

PI628144 AUS28321 Iran, Khorasan 0.65 0.9 R

Sönmez Turkey, Eskisehir 0.98 1.7 R

Silverstar Australia, Victoria 1.41 3.1 MR

PI628119 AUS28308 Iran,Esfahan 1.43 3.2 MR

PI621458 AUS28451 Iran, East Azarbaijan 1.51 3.5 MR

PI624327 AUS28470 Iran,Kordestan 1.52 3.6 MR

PI627713 AUS28281 Iran,Esfahan 1.61 4.0 MR

PI624822 AUS28688 Iran,Ilam 1.62 4.0 MR

PI624162 AUS28401 Iran, Kermanshah 1.90 5.7 MRMS

PI628135 AUS28318 Iran,Esfahan 1.93 5.9 MRMS

PI623979 Iran,Hamadan 2.03 6.6 MRMS

PI623428 AUS28297 Iran, East Azarbaijan 2.04 6.7 MRMS

PI623501 AUS28342 Iran,Ilam 2.05 6.7 MRMS

PI628045 AUS28302 Iran,Esfahan 2.08 7.0 MRMS

PI624861 AUS28707 Iran,Ilam 2.09 7.0 MRMS

PI624282 AUS28430 Iran, Kermanshah 2.11 7.2 MRMS

PI624253 AUS28414 Iran,Hamadan 2.17 7.7 MS

NSGC12570 AUS28322 Iran, Khorasan 2.18 7.9 MS

PI628047 AUS28303 Iran, Kermanshah 2.35 9.5 MS

PI628116 AUS28307 Iran,Esfahan 2.36 9.6 MS

PI627824 AUS28285 Iran, Khorasan 2.38 9.7 MS

PI628120 AUS28309 Iran,Esfahan 2.39 10.0 MS

PI623442 Iran, Kerman 2.40 10.0 MS

PI624686 AUS28638 Iran, Kermanshah 2.43 10.4 MS

PI623441 Iran,ChaharMahall and Bakhtiari 2.44 10.4 MS

PI628151 AUS28324 Iran, East Azarbaijan 2.45 10.6 MS

PI624286 AUS28433 Iran, Kermanshah 2.52 11.4 S

PI623425 AUS28295 Iran,Markazi 2.54 11.6 S

PI624009 AUS28389 Iran, Kermanshah 2.59 12.4 S

PI624860 AUS28706 Iran,Ilam 2.64 13.1 S

Kutluk Turkey, Eskisehir 2.70 13.9 S

PI628100 AUS28304 Iran, Khorasan 2.78 15.1 S

PI624821 AUS28687 Iran,Ilam 2.92 17.5 S

Bezostaya Russia 3.20 23.4 S

PI624815 AUS28685 Iran,Ilam 3.26 25.0 S

F Probability <0.001

Mean 2.16

LSD(5 %) 0.73

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The data (cysts/ plant) were transformed logarithmically (ln[x + 1]) prior to analysis of variance (ANOVA) with LSDs calculated to determine treatment effects using GenStat (17th edition) statistical software (VSN International2014). Resistance reactions of the accessions were compared with reference cultivars and allocated into provisional resistance groups. Cultivars statistically similar to the most resistant cul-tivar were classified as resistant (R), culcul-tivars that produced significantly more cysts than the most resistant cultivar were classified as moderately resistant (MR), cultivars that pro-duced significantly more cysts than the most resistant cultivar but were not significantly different to the MR reference cv. Silverstar were classified as moderately resistant to moderate-ly susceptible (MRMS), cultivars that produced significantmoderate-ly more cysts than cv. Silverstar were classified as moderately susceptible (MS) and cultivars that were statistically similar to the susceptible reference cv. Bezostaya were classified as sus-ceptible (S).

Resistance reactions of the 31 landraces ranged from resis-tant to susceptible (Table1). PI628144 had the lowest number of cysts, a number similar to the resistant reference cv. Sönmez and was therefore grouped as resistant to H. filipjevi. PI628119, PI621458, PI624327, PI627713 and PI624822 all had counts similar to the moderately resistant reference cv. Silverstar. Twenty-five landraces had significantly higher cyst numbers than cv. Sönmez, with seven similar to the suscepti-ble reference cv. Bezostaya. The remaining 18 accessions sup-ported intermediate levels of cyst production.

The Iranian landraces evaluated in this study have the po-tential to be useful sources of resistance to the Haymana pop-ulation of H. filipjevi with six wheat accessions provisionally identified as resistant or moderately resistant. Additional eval-uation of these accessions for resistance to H. filipjevi will be necessary to fully establish their R or MR classifications. However, a recent evaluation of germplasm from the International Winter Wheat Improvement Program for resistance to H. filipjevi also found 47 % of Iranian accessions were resistant or highly resistant to the Haymana population (Dababat et al.2014). Importantly, PI628144 (syn. AUS28321), PI621458 (syn. AUS28451) and PI624327 (syn. AUS28470) have also been reported as resistant to the root lesion nematode Pratylenchus thornei with PI621458 also moderately resistant to Russian wheat aphid (Diuraphis noxia) biotype 2 (Sheedy and Thompson2009).

Specific genes conferring resistance to H. filipjevi have not yet been identified, however several genes conferring resis-tance to H. avenae in wheat cultivars (Cre genes) have been catalogued (McIntosh et al.2003) and subsequently evaluated for resistance to H. filipjevi. It should be noted that several H. filipjevi populations occur in Turkey (Dababat et al.2014; Toktay et al.2013) and reactions of the cultivars carrying these Cre genes are not consistent across all of the populations (Dababat et al.2014; Toktay et al.2012,2013). Heterodera

avenae has numerous pathotypes that react differentially to each of the Cre genes, and it may be that some of the apparent inconsistency is due to the existence of H. filipjevi pathotypes. Several studies have shown differ-ential reactions of H. filipjevi populations to putative resistant cereal germplasm (Ozarslandan et al.2010; Toktay et al.2013; Wu et al.2016) and in this circumstance, the Cre genes may only confer resistance to some H. filipjevi pathotypes. It is also possible that some of the Cre gene-carrying cultivars also carry unidentified H. filipjevi resistance genes, further compli-cating the process of determining if some Cre genes provide broad spectrum resistance across the H. avenae complex.

The accessions that have resistance and moderate resis-tance in this study provide additional genetic resources for wheat breeding programs and offer the opportunity to not only improve resistance to H. filipjevi in commercial cultivars, but also develop cultivars with multiple disease resistances. It would be valuable to re-evaluate the resistance of these culti-vars to the Haymana H. filipjevi population, and to other H. filipjevi populations and to initiate targeted studies to identify both quantitatively and molecularly the H. filipjevi resistance in these accessions.

The authors thank CIMMYT for providing wheat acces-sions for the study, TUBİTAK for supporting the study finan-cially (Project Number: 105G013) and A. Amer Dababat (CIMMYT, Turkey) for commenting on the manuscript.

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Şekil

Table 1 Mean number of Heterodera filipjevi cysts per plant, provisional resistance group and origin of Iranian wheat landrace accessions ( 1 United States Department of Agriculture accession number; 2 Australian Grains Gene Bank accession number; 3 Back-t

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