scholarly journals The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes

2018 ◽  
Author(s):  
Rick Masonbrink ◽  
Tom R. Maier ◽  
Usha Muppiral ◽  
Arun S. Seetharam ◽  
Etienne Lord ◽  
...  

AbstractHeterodera glycines, commonly referred to as the soybean cyst nematode (SCN), is an obligatory and sedentary plant parasite that causes over a billion-dollar yield loss to soybean production annually. Although there are genetic determinants that render soybean plants resistant to certain nematode genotypes, resistant soybean cultivars are increasingly ineffective because their multi-year usage has selected for virulentH. glycinespopulations. The parasitic success ofH. glycinesrelies on the comprehensive re-engineering of an infection site into a syncytium, as well as the long-term suppression of host defense to ensure syncytial viability. At the forefront of these complex molecular interactions are effectors, the proteins secreted byH. glycinesinto host root tissues. The mechanisms of effector acquisition, diversification, and selection need to be understood before effective control strategies can be developed, but the lack of an annotated genome has been a major roadblock. Here, we use PacBio long-read technology to assemble aH. glycinesgenome of 738 contigs into 123Mb with annotations for 29,769 genes. The genome contains significant numbers of repeats (34%), tandem duplicates (18.7Mb), and horizontal gene transfer events (151 genes). Using previously published effector sequences, the newly generatedH. glycinesgenome, and comparisons to other nematode genomes, we investigate the evolutionary mechanisms responsible for the emergence and diversification of effector genes.

Author(s):  
Rick Masonbrink ◽  
Tom Maier ◽  
Matthew Hudson ◽  
Andrew Severin ◽  
Thomas Baum

The soybean cyst nematode (Heterodera glycines) is a sedentary plant parasite that exceeds a billion dollars in yield losses annually. It has spread across the soybean-producing world, emerging as the primary pathogen of soybeans. This problem is exacerbated by H. glycines populations overcoming the limited sources of natural resistance in soybean and by the lack of effective and safe alternative treatments. Although there are genetic determinants that render soybean plants resistant to certain nematode genotypes, resistant soybean cultivars are increasingly ineffective because their multi-year usage has selected for virulent H. glycines populations. Successful H. glycines infection relies on the comprehensive re-engineering of soybean root cells into a syncytium, as well as the long-term suppression of host defenses to ensure syncytial viability. At the forefront of these complex molecular interactions are effectors, the proteins secreted by H. glycines into host root tissues. The mechanisms that control genomic effector acquisition, diversification, and selection are important insights needed for the development of essential novel control strategies. As a foundation to obtain this understanding, we developed a nine scaffold, 158Mb pseudomolecule assembly of the H. glycines genome using PacBio, Chicago, and Hi-C sequencing. An annotation of 22,465 genes was predicted using a Mikado pipeline informed by published short- and long-read expression data. Here we present results from our assembly and annotation of the H. glycines genome.


Genetics ◽  
1997 ◽  
Vol 146 (4) ◽  
pp. 1311-1318 ◽  
Author(s):  
Ke Dong ◽  
Charles H Opperman

A genetic analysis of parasitic ability in the soybean cyst nematode Heterodera glycines was performed. To identify and characterize genes involved in parasitism, we developed three highly inbred H. glycines lines, OP20, OP25 and OP50, for use as parents for controlled crosses. Through these crosses, we have identified genes in the inbred parents that control reproduction of the nematode on hosts that carry resistance genes. These genes, designated as ror-* for reproduction on a resistant host, segregate in a normal Mendelian fashion as independent loci. Host range tests of F1 generation progeny indicated that at least one parasitism gene in both the OP20 and OP50 lines for host PI 88788 was dominant. Parasitism genes in OP50 for hosts “Peking” and PI 90763 are recessive. Two types of single female descent populations, a single backcrossed BC1F2-derived and a double backcrossed BC2F1-derived, were established on the susceptible soybean cultivar “Lee 68.” Host range tests for parasitism in these lines demonstrated the presence of two independent genes in OP50, one for host PI 88788 designated ror-1 and one for host PI 90763 designated ror-2. OP20 carries two independent genes for parasitism on PI 88788, designated as alleles kr3 and kr4.


Plant Disease ◽  
2009 ◽  
Vol 93 (3) ◽  
pp. 319-319 ◽  
Author(s):  
J. Zheng ◽  
Y. Zhang ◽  
X. Li ◽  
L. Zhao ◽  
S. Chen

The soybean cyst nematode (SCN), Heterodera glycines Ichinohe, is a destructive pest of soybean. Damage to soybean by SCN was first reported from northeastern China in 1899 (1). SCN has been documented in Anhui, Beijing, Hebei, Heilongjiang, Henan, Jiangsu, Jilin, Liaoning, Neimenggu, Shaanxi, Shandong, and Shanxi provinces in mainland China (1). These provinces are situated in the Heilongjiang and Songhuajing valleys in northeastern China and the eastern region of the Yangtze and Yellow rivers in northern China and have cold to temperate climates. In June of 2008, cyst-forming nematodes were detected in two soybean-growing areas of Hangzhou and Xiaoshan in Zhejiang Province, in subtropical eastern China. The soybean plants at the Hangzhou site showed symptoms of stunting and chlorosis, whereas no aboveground or root symptoms were observed on soybean plants at the Xiaoshan site, except for the presence of SCN females on the roots. The two populations had the same morphological and molecular characters. The cysts were lemon shaped with posterior protuberance, ambifenestrate, underbridge and bullae strongly developed, and lateral field of second-stage juveniles consisted of four incisures. The key morphometrics of cysts were fenestra length (41 to 52 μm) and width (33 to 48 μm), vulval silt (47 to 55 μm), and underbridge length (79 to 94 μm), all of which were coincident with that of SCN (2). Amplification of rDNA-internal transcribed spacer (ITS) region using primers TW81 (5′-GTT TCC GTA GGT GAA CCT GC-3′) and AB28 (5′-ATA TGC TTA AGT TCA GCG GGT-3′) yielded a PCR fragment of approximately 1,030 bp. The digestion patterns of the PCR fragments of the ITS region with AluI, AvaI, CfoI, MvaI, and RsaI showed identical restriction profiles to H. glycines (3), and the sequences exhibited 100% similarity with those of H. glycines isolates, Accession No. AY667456 from GenBank. Morphological and molecular identification confirmed that the two populations of cyst-forming nematodes from Zhejiang are SCN. To our knowledge, this is the first report of SCN in Zhejiang, now the most southern location in mainland China with confirmed infestation of SCN. References: (1) Z. X. Liu et al. Int. J. Nematol. 7:18, 1997. (2) R. H. Mulvey. Can. J. Zool. 50:1277, 1972. (3) J. Zheng et al. Russ. J. Nematol. 8:109, 2000.


BMC Genomics ◽  
2019 ◽  
Vol 20 (1) ◽  
Author(s):  
Rick Masonbrink ◽  
Tom R. Maier ◽  
Usha Muppirala ◽  
Arun S. Seetharam ◽  
Etienne Lord ◽  
...  

2006 ◽  
Vol 33 (11) ◽  
pp. 991 ◽  
Author(s):  
Ryan M. Steeves ◽  
Tim C. Todd ◽  
Juliane S. Essig ◽  
Harold N. Trick

The soybean cyst nematode (SCN), Heterodera glycines, is the major disease-causing agent limiting soybean production in the USA. The current management strategy to reduce yield loss by SCN involves the deployment of resistant soybean cultivars and rotation to non-host crops. Although this management scheme has shown some success, continued yearly yield loss estimates demonstrate the limitations of these techniques. As a result, new control strategies are needed to complement the existing methods. Reported here is a novel method of SCN control that utilises RNA interference (RNAi). Transgenic soybeans were generated following transformation with an RNAi expression vector containing inverted repeats of a cDNA clone of the major sperm protein (MSP) gene from H. glycines. The accumulation of MSP-specific short interfering RNA (siRNA) molecules were detected by northern blot analysis of transgenic soybeans. T0 plants displaying MSP siRNA accumulation were deployed in a bioassay to evaluate the effects of MSP interfering molecules on H. glycines reproduction. Bioassay data has shown up to a 68% reduction in eggs g–1 root tissue, demonstrating that MSPi transgenic plants significantly reduced the reproductive potential of H. glycines. An additional bioassay evaluating progeny nematodes for maintenance of reproductive suppression indicated that progeny were also impaired in their ability to successfully reproduce, as demonstrated by a 75% reduction in eggs g–1 root tissue. The results of this study demonstrate the efficacy of an RNAi-based strategy for control of the soybean cyst nematode. In addition, these results may have important implications for the control of other plant parasitic nematodes.


Plant Disease ◽  
2021 ◽  
Author(s):  
Jingsheng Chen ◽  
Yuanyuan Zhou ◽  
Yuanyuan Wang ◽  
Haiyan Fan ◽  
Xiaoyu Liu ◽  
...  

Knowledge about virulent phenotypes of Heterodera glycines Ichinohe, 1952 (soybean cyst nematode, SCN) is essential for breeding resistant cultivars and managing this nematode. Heilongjiang Province is the major soybean producing region in China. SCN has been reported in 63 regions in Heilongjiang Province. To determine the prevalence and virulence of phenotypes of SCN, 112 soil samples were collected from soybean fields throughout the province in 2015. SCN was detected in 62 samples (55.4%) of these samples, with population densities ranging from 150 to 41,750 eggs and juveniles per 100 cm3 of soil. Eleven HG types, namely HG 0, 1.2.3.5.7, 1.2.3.7, 1.3.4.7, 1.3.7, 2, 2.5.7, 2.7, 6, 6.7, and 7, were detected. The percentages of SCN populations with female indices greater than ten ranged from 4.8% for PI 437654 to 64.5% for PI 548316. This is the first report of seven of the HG types from Heilongjiang. These results provide guidance for breeding efforts and control strategies to combat SCN.


Plant Disease ◽  
2013 ◽  
Vol 97 (6) ◽  
pp. 852-852 ◽  
Author(s):  
H. Shi ◽  
J. Zheng

Soybean cyst nematode (SCN) (Heterodera glycines) commonly infests soybean (Glycine max), but has also been reported to infest haricot bean, mung bean, adzuki bean, some species of Lespedeza and Melilotus (3), purple deadnettle (Lamium purpureum), henbit (Lamium amplexicaule), field pennycress (Thlaspi arvense), and shepherd's-purse (Capsella bursa-pastoris) (4). During 2009 to 2011, a survey for plant parasitic nematodes on tobacco was made in Xuchang, Henan Province, central China. Thirty six percent of 50 tobacco fields showed yellowing symptoms, and females and cysts of cyst-forming nematode were observed in the yellowing tobacco roots. The cysts were characterized by a lemon shape, with posterior protuberance, ambifenestrate, bullae, and underbridge present. The key morphometrics of cysts were fenestra length (38 to 44 μm) and width (34 to 40 μm), vulval silt (41 to 50 μm), and underbridge length (73 to 99 μm), all of which were similar to SCN (1). DNA was extracted by putting a single cracked cyst collected from the tobacco root to a 0.2-ml Eppendorf tube containing 10 μl double distilled water, 8 μl 10 × PCR Buffer (Mg–), and 2 μl of proteinase K (600 μg/ml) and frozen at –70°C for 30 min, then incubated at 65°C for 1 h and at 95°C for 10 min. After centrifugation at 12,000 rpm for 2 min, the DNA suspension was used for PCR amplification. Primers TW81 (5′-GTTTCCGTAGGTGAACCTGC-3′) and AB28 (5′-ATATGCTTAAGTTCAGCGGGT-3′) were used to amplify the rDNA internal transcribed spacer (ITS) region, and a PCR fragment of 1,030 bp was obtained. The sequence (GenBank Accession No. JX561139) showed 99% similarity to H. glycines strain Hg1-Ark1 (EF611124). Duplex PCR containing the universal primers D2A (5′-ACAAGTACCGTGAGGGAAAGTTG-3′), D3B (5′-TCGGAAGGAACCAGCTACTA-3′) and SCAR primers SCNFI (5′-GGACCCTGACCAAAAAGTTTCCGC-3′), SCNRI (5′-GGACCCTGACGAGTTATGGGCCCG-3′), obtained a 477-bp fragment, which is specific for SCN populations (2). Based on both morphological and molecular identification, the populations of cyst-forming nematodes on tobacco from Henan, China were confirmed as SCN. Pathogenicity tests were conducted on 30 each of 50-day-old tobacco and 5-day-old soybean plants (one plant per pot), respectively, by adding 2 ml of a suspension of 1,000 eggs and J2 of cysts collected from tobacco roots. After 35 days, 20 to 35 white females could be detected in each of the tobacco roots, and the yellowing symptom on almost all of tobacco plants was observed. Although infection on soybean plants was observed, the nematodes infected in roots was just 10 to 20 per pot, and they all stayed in the infective J2 stage. Except for one J3 until 48 dpi, no mature females could be found, and the nematode population could not reproduce on soybean tested. This suggests that the cyst nematode population from tobacco is a new pathotype of SCN. To our knowledge, this is the first report of SCN parasitized on tobacco in naturally infected fields, which is a potential threat to tobacco growth and should attract worldwide attention. References: (1) R. H. Mulvey. Can. J. Zool. 50:1277, 1972. (2) S. Ou et al. Nematology 10:397, 2008. (3) R. D. Riggs. In: Biology and Management of the Soybean Cyst Nematode, p. 107-114, 1992. (4) R. Venkatesh et al. Weed Technol. 14:156, 2000.


2003 ◽  
Vol 16 (5) ◽  
pp. 439-446 ◽  
Author(s):  
Sadia Bekal ◽  
Terry L. Niblack ◽  
Kris N. Lambert

Parasitism genes from phytoparasitic nematodes are thought to be essential for nematode invasion of the host plant, to help the nematode establish feeding sites, and to aid nematodes in the suppression of host plant defenses. One gene that may play several roles in nematode parasitism is chorismate mutase (CM). This secreted enzyme is produced in the nematode's esophageal glands and appears to function within the plant cell to manipulate the plant's shikimate pathway, which controls plant cell growth, development, structure, and pathogen defense. Using degenerate polymerase chain reaction primers, we amplified and cloned a chorismate mutase (Hg-cm-1) from Heterodera glycines, the soybean cyst nematode (SCN), and showed it had CM activity. RNA in situ hybridization of Hg-cm-1 cDNA to SCN sections confirms that it is specifically expressed in the nematodes' esophageal glands. DNA gel blots of genomic DNA isolated from SCN inbred lines that have differing virulence on SCN resistant soybean show Hg-cm-1 is a member of a polymorphic gene family. Some Hg-cm family members predominate in SCN inbred lines that are virulent on certain SCN resistant soybean cultivars. The same polymorphisms and correlation with virulence are seen in the Hg-cm-1 expressed in the SCN second-stage juveniles. Based on the enzymatic activity of Hg-cm-1 and the observation that different forms of the mutase are expressed in virulent nematodes, we hypothesize that the Hg-cm-1 is a virulence gene, some forms of which allow SCN to parasitize certain resistant soybean plants.


Plant Disease ◽  
2021 ◽  
Vol 105 (1) ◽  
pp. 31-33 ◽  
Author(s):  
Heonil Kang ◽  
Hyoungrai Ko ◽  
Donggeun Kim ◽  
Insoo Choi

Soybean cyst nematode (Heterodera glycines, SCN) is the most harmful pathogen of soybean (Glycine max (L.) Merr.) worldwide. In 2016, a new soybean-parasitic cyst nematode, Heterodera sojae (the white soybean cyst nematode) was found parasitizing the roots of soybean plants in Korea. To investigate the distribution and population density of H. sojae, 943 soil samples were collected from soybean fields in all nine provinces in Korea in 2017 to 2018. Cyst nematodes were detected in 343 samples (36.4%) from eight of the nine provinces, except the island of Jeju province. Among the 343 samples, H. glycines was found in 227 samples (66.2%), H. sojae in 95 samples (27.7%), and 21 samples (6.1%) were infested with both H. sojae and H. glycines. Wide distribution of H. sojae in soybean fields indicates that H. sojae is an important cyst nematode species parasitizing soybean together with H. glycines.


Agronomy ◽  
2021 ◽  
Vol 11 (1) ◽  
pp. 146
Author(s):  
Leonardo F. Rocha ◽  
Karla L. Gage ◽  
Mirian F. Pimentel ◽  
Jason P. Bond ◽  
Ahmad M. Fakhoury

The soybean cyst nematode (SCN; Heterodera glycines Ichinohe) is a major soybean-yield-limiting soil-borne pathogen, especially in the Midwestern US. Weed management is recommended for SCN integrated management, since some weed species have been reported to be hosts for SCN. The increase in the occurrence of resistance to herbicides complicates weed management and may further direct ecological–evolutionary (eco–evo) feedbacks in plant–pathogen complexes, including interactions between host plants and SCN. In this review, we summarize weed species reported to be hosts of SCN in the US and outline potential weed–SCN management interactions. Plants from 23 families have been reported to host SCN, with Fabaceae including most host species. Out of 116 weeds hosts, 14 species have known herbicide-resistant biotypes to 8 herbicide sites of action. Factors influencing the ability of weeds to host SCN are environmental and edaphic conditions, SCN initial inoculum, weed population levels, and variations in susceptibility of weed biotypes to SCN within a population. The association of SCN on weeds with relatively little fitness cost incurred by the latter may decrease the competitive ability of the crop and increase weed reproduction when SCN is present, feeding back into the probability of selecting for herbicide-resistant weed biotypes. Therefore, proper management of weed hosts of SCN should be a focus of integrated pest management (IPM) strategies to prevent further eco–evo feedbacks in the cropping system.


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