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Article

Resistance Analysis of a Soybean Cultivar, Nongqing 28 against Soybean Cyst Nematode, Heterodera glycines Ichinohe 1952

by
Changjun Zhou
1,
Yanfeng Hu
2,*,
Yingpeng Han
3,
Gang Chen
1,
Bing Liu
1,
Jidong Yu
1,
Yaokun Wu
1,
Jianying Li
1,
Lan Ma
1 and
Jian Wei
4,*
1
Soybean Molecular Breeding Faculty Daqing Branch, Heilongjiang Academy of Agricultural Science, Daqing 163316, China
2
Key Laboratory of Black Soils Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin 150081, China
3
Key Laboratory of Soybean Biology in Chinese Ministry of Education, Key Laboratory of Soybean Biology and Breeding/Genetics of Chinese Agriculture Ministry, Northeast Agricultural University, Harbin 150030, China
4
School of Agriculture, Jilin Agricultural University, Changchun 130118, China
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(9), 1964; https://doi.org/10.3390/agronomy14091964 (registering DOI)
Submission received: 21 July 2024 / Revised: 26 August 2024 / Accepted: 26 August 2024 / Published: 30 August 2024
(This article belongs to the Special Issue Functional Genomics and Molecular Breeding of Soybeans)
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Abstract

:
The soybean cyst nematode (SCN), Heterodera glycines Ichinohe, 1952, is one of the most destructive plant-parasitic nematodes in soybean production worldwide. The use of resistant soybean is the most effective alternative for its management. However, SCN-resistant soybean cultivars with increased yield and favorable agronomic traits remain limited in the market. Here, we developed a new SCN-resistant soybean cultivar Nongqing 28 from the cross of the female parent cultivar An 02-318 and a male parent line F2 (Hei 99-980 × America Xiaoheidou). Resistance evaluation suggested that Nongqing 28 displayed stable resistance to SCN race 3 in pot assays and the 5-year field experiments, including inhibition of SCN development and reduction in female and cyst numbers. The average yields of Nongqing 28 were 2593 kg/ha and 2660 kg/ha in the 2-year regional trails and the 1-year production trials, with a yield increase of 6.2% and 8.1% compared with the local cultivar Nengfeng 18, respectively. The average seed fat contents in Nongqing 28 reached 21.26%. Additionally, RNA-seq analysis revealed that the resistance of Nongqing 28 to SCN infection is involved in pathogen perception and defense activation, such as reactive oxygen species burst, calcium-mediated defense signaling, hormonal signaling, the MAPK signaling cascade, and phenylpropanoid biosynthesis. In summary, this study provides a detailed characterization of a novel SCN-resistant soybean cultivar with high oil and yield potential.

1. Introduction

Soybean (Glycine max (L.) Merrill) is an important legume crop that supplies essential oils and vegetable proteins for humans and animals and serves as a source of biofuel. However, soybean yield is substantially impacted by several biotic constraints, including soybean cyst nematode (SCN), Heterodera glycines Ichinohe, 1952. Currently, SCN has spread worldwide and has emerged as one of the most destructive pathogens for soybean production globally [1,2]. In the United States, it was previously estimated that SCN caused up to USD 32 billion of soybean yield losses from 1996 through 2016 [3]. In China, more than USD 120 million of soybean production is lost annually due to SCN infestation [1]. Notably, this pathogen is particularly prevalent in two main soybean-producing regions, the Huang-Huai Valleys in Central-East China and Northeast China [4,5].
To reduce the yield losses caused by SCN, the use of cultural, chemical, and biological methods are the recommended management actions [6]. Generally, rotating soybean with non-host plants such as corn (Zea mays. L.) or wheat (Triticum aestivum. L.) is partially effective because SCN cysts display resistance to adverse conditions, protecting the developing eggs for many years in soil. Additionally, crop rotation can lead to a decrease in the total soybean production. The use of chemical nematicides is limited and, in some cases, prohibited because of their harmful effect on the environment. In this context, the cultivation of SCN-resistant soybean cultivars represents the most economically and environmentally viable method to control SCN in the field [6].
Surveys indicate that most of the commercial SCN-resistant soybean varieties are derived from limited resistance sources such as PI 548402 (Peking), PI 88788, and PI 437654 [7,8]. Rhg1 (Peking-type rhg1-a and PI88788-type rhg1-b) and Rhg4 (GmSHMT08) are two major-effect quantitative trait loci (QTL) conferring the resistance of these varieties to SCN [9,10]. However, overuse of these resistant cultivars has led to a genetic shift in SCN populations. For example, some virulent SCN races are capable of overcoming Peking-type resistant sources [6]. To broaden the genetic basis for breeding SCN-resistant cultivars, considerable efforts have been made to identify new resistant varieties and QTLs. For example, few resistant soybean sources lacking the Rhg1 or Rhg4 loci such as PI 567516C [11] and Pingliang Xiaoheidou [12] have been identified. To date, more than 200 QTLs, including new SCN-resistant QTLs such as qSCN-PL10 [12] and SCN_7_1 [13], have been reported and mapped to 20 chromosomes [1].
Heilongjiang is the largest province in total soybean areas planted, contributing to over 40% of the total soybean production in China. Since the launch of the ‘Soybean Planting Expansion Plan’, Heilongjiang has continuously increased its total planting area of soybeans. In 2022, it reached 4.93 million hectares from 3.90 million hectares in 2021, representing a 17.1 percent increase. Heilongjiang also has a longer history of SCN infestation, with SCN first reported in 1899 in Anda County of Heilongjiang [14]. Survey data demonstrated that the infestation of SCN in Heilongjiang has spread to at least 63 soybean-planting counties [15,16]. Heilongjiang possesses highly genetically diverse SCN populations, including eleven different HG types [5,16]. Moreover, it has been reported that the continuous planting of a single type of resistant cultivar such as Peking and Franklin has resulted in shifts in dominant SCN populations in this region [17].
The publicly available utilized resistance sources are limited for developing soybean resistant varieties in China [16,17,18]. Although more than 30 commercially registered soybean varieties with SCN resistance developed in Heilongjiang since 1990 [1,18], few SCN-resistant varieties with increased yield and favorable agronomic traits have been reported [19]. With this objective, we developed a new SCN-resistant soybean cultivar, Nongqing 28, from a cross between the female parent cultivar An 02-318 and a male parent line F2 (Hei 99-980 × America Xiaoheidou). We determined the characteristic of SCN resistance and agronomic traits in Nongqing 28. Furthermore, we conducted transcriptomic analysis to gain insights into the molecular mechanisms of SCN resistance in Nongqing 28.

2. Materials and Methods

2.1. Breeding Nongqing 28 and Selection

Soybean pedigree breeding was employed to develop Nongqing 28 through crosses between An 02-318 as the male parent and the female parental line F2 (Heihe 99-980 × America Xiaoheidou) in Anda County, Heilongjiang (Figure 1). The SCN-resistant cultivar An02-318 was developed from the cross of the high-yielding parent Hefeng 25 and the SCN-resistant parent Hartwig before 2006 by the Daqing branch of the Heilongjiang Academy of Agricultural Sciences. The hybrid seeds of the F2 (F2-1) generation of Heihe 99-980 × America Xiaoheidou was produced in 2006. The cross of An 02-318 and an individual F2-1 line of Hei 99-980 × America Xiaoheidou was made by artificial hybridization in Anda, and F0 seeds were harvested in the fall of 2007. Seeds of subsequent generations from F1 to F5 were self-bred in Anda. From 2012 to 2014, the seeds of generations from F6 to F8 were planted in SCN-infested (Race 3) fields for disease resistance testing in Daqing. During 2015–2017, the seeds of F8 generations were collected for field tests. Finally, Nongqing 28 is a highly homozygous recombinant inbred line derived from an individual F13 generation single plant through 5-year screening in SCN-infested fields, 2-year regional trials (2018–2019), and a 1-year production trial (2019). Nongqing 28 (Reg. No. ‘Heishendou 20200006’) was released by the Daqin branch of the Heilongjiang Academy of Agricultural Sciences in 2020 as a new soybean cultivar due to its high seed yield potential and SCN resistance in Heilongjiang Province.

2.2. Determination of Seed Yield and Agronomic Traits in Field Trials

During 2018–2019, seed yield and agronomic trails were assessed through regional and production trials at different locations in Heilongjiang Province. Seeds were planted between 4 May and 11 May and harvested between 14 September and 23 September. Sowing fertilization consisted of 30~45 kg N ha−1, 60~80 kg ha−1 P2O5, and 45~60 kg K2O ha−1. In 2018, the regional trials were performed at six locations (Anda Dapeng Seeds Co., Ltd. (Anda, China), Longjiang Branch of Qishan Seeds Co., Ltd. (Harbin, China), Daqing Seeds Management Bureau, Dumeng Seeds Management Bureau, Tailai Seeds Station, and Qiqihar Branch of Heilongjiang Academy of Agricultural Sciences using soybean cultivar Nengfeng 18 as the control. In 2019, the regional trials were performed at five locations including Anda Dapeng Seeds Co., Ltd., Longjiang Branch of Qishan Seeds Co., Ltd., Daqing Seeds Management Bureau, Tailai Seeds Station, and Qiqihar Branch of Heilongjiang Academy of Agricultural Sciences. The production trials were performed at five locations including Anda Dapeng Seeds Co., Ltd., Longjiang Branch of Qishan Seeds Co., Ltd., Qinggang Experimental Station of Beifeng Seeds Co., Ltd. (Qinggang, Suihua, China), Tailai Seeds Station, and Qiqihar Branch of Heilongjiang Academy of Agricultural Sciences, and Nengfeng 18 served as the control. For all field trials, each trial location employed a randomized complete design with three plots (three replicates) in each year. The seed yield was converted based on the production of each plot with about 20 m2 in regional trials and 300 m2 in production trials.
Seeds were collected for each regional trial location during harvest and analyzed for protein and oil content. The crude protein content in soybean seeds was determined according to the national standards of China (GB2905-82) using the Semi-micro Kjeldahl method. The seed crude fats were measured according to the method described in the national standards of China (GB 2906-82).

2.3. Assessment of SCN Resistance

Evaluation of SCN resistance was performed by the Daqing branch of Heilongjiang Academy of Agricultural Sciences in SCN-infested fields in Anda and Daqing Counties. For the field assay, soybean seeds were planted in SCN-infested fields in May during 2018–2022, with the susceptible soybean cultivar Lee used as the control. Sowing fertilization during sowing consisted of 40 kg N ha−1, 65 kg ha−1 P2O5, and 52 kg K2O ha−1. The predominant SCN population in these soybean fields was identified to be HG Type 0 (Race 3) using the race scheme [20] and the HG type test [21]. Approximately 45 days after germination, soybean plants were harvested, and SCN females were extracted from both roots and soil. The numbers of females were counted with a stereomicroscope. The female index (FI) was calculated as follows: FI = (average number of females on each soybean cultivar/average number of females on the susceptible check Lee) × 100 [21].
The pot assay was conducted in a greenhouse at the Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, in August 2023. SCN HG Type 0 (Race 3) was used as inoculum. This SCN population was originally isolated from an SCN-infested field in Daqing County, Heilongjiang. To acquire sufficient inoculums for the assessment of SCN resistance, HG Type 0 was maintained on Hefeng 50 under greenhouse conditions at 22–28 °C and a 16 h light/8 h dark photoperiod. SCN cysts were extracted from the SCN-infected soil and soybean roots using floating sieves (850 µm pore and 250 µm pore). Next, cysts were manually crushed on the surface of a sieve (75 µm pore) with a rubber stopper to release intact eggs. Subsequently, the eggs were collected on a 25 µm pore sieve and incubated in a hatching box at 26 °C for 3–6 days to prepare inoculums. Seeds of Nongqing 28, PI 437645, Hefeng 50, and Lee were planted in pots (7.0 cm diameter × 10.3 cm height) containing a mixture of sterilized sand and soil (2:1). After growing for two weeks, each seedling was inoculated with 1000 second-stage juveniles (J2) of HG Type 0 and maintained under controlled greenhouse conditions. Hefeng 50 and Lee were used as the susceptible controls, while PI 437654 was set as the resistant control. The plants were watered daily, and in addition, the Hoagland modified nutrient solution (Coolaber, Beijing, China) was applied every five days to support seedling growth and development. At 5 and 10 days post inoculation (dpi), nematode development in the collected roots was surveyed by acid fusion staining [22]. The number of nematodes at the different developmental stages (J2, J3, and/or J4) was counted using a stereomicroscope. At 21 dpi, the white females on roots for each plant were count with a stereomicroscope. Ten replicates were included at each time point, and the experiment was repeated three times.

2.4. RNA Sample Preparation and Library Construction and Illumina Sequencing Analysis

Two-week-old Nongqing 28 plants were inoculated with SCN HG Type 0, with each plant using 1000 J2. At 10 dpi, the roots from six soybean plants were pooled as one biological replicate, and total three biological roots samples from both SCN-infected and non-infected plants were prepared for RNA extraction and library construction. Total RNA was extracted using a commercial Plant RNA Extraction Mini Kit 451 (ONREW, Foushan, China) according to the manufacturer’s instructions. RNA integrity, purity, and concentrations were assessed using an Agilent 4200 system (Agilent Technologies, Waldbron, Germany) with Nanodrop One (Thermo Fisher Scientific, Waltham, MA, USA). Library construction and sequencing were performed by Guangdong Meg Gene Biotechnology Co., LTD (Guangzhou, China) using the illumina platform with 150 bp paired-end reads. High-quality reads were mapped against the Williams 82 soybean reference genome (Glycine max Wm82.a4.v1) with Hisat2 (v2.2.1). Gene expression was assessed using DESeq2 (v1.34.0). Only those genes with a false discovery rate (FDR) ≤ 0.05 and |log2(fold change)| ≥ 1 were considered differentially expressed genes (DEGs).

2.5. Quantitative Real-Time (qRT)-PCR Analysis

Total RNA was purified from soybean roots using an RNAPrep Pure Micro Kit (TianGen Biotech, Beijing, China) following the manufacturer’s instructions, including a DNase treatment step. First-strand cDNA was synthesized from 1.0 μg of total RNA using FastKing gDNA Dispelling RT SuperMix FastKing Kit (TianGen Biotech, Beijing, China). PCR reactions were performed in the LightCycler® 480 System with AceQ qPCR SYBR Green Master Mix (Vazyme, Nanjing, China) according to the manufacturer’s procedure. The primers used for qRT-PCR are listed in Supplementary Table S3. PCR cycles began with 5 min at 95 °C, followed by 40 cycles of 10 s at 95 °C and 30 s at 60 °C. The 2−∆∆Ct method was applied to calculate the relative expression of specific genes using GmUBQ3 as a reference control. All experiments were conducted with three independent biological replicates, each with three technical replicates.

2.6. Data Analysis

Data were subjected to one-way ANOVA using SPSS version 17.0 software (Chicago, IL, USA). Tukey’s HSD test (p < 0.05) was used for overall pairwise comparisons. The error bars in the figures represent the SE of means, and the significance level was set at p < 0.05.

3. Results

3.1. Main Characteristics of Nongqing 28

The main agronomic traits of Nongqing 28 were investigated in two continuous years (2018 and 2019). Nongqing 28 has white flowers, round leaves, gray pubescence, sickle-shaped pods, and a determinate growth habit. The growth period of Nongqing 28 is about 123 days, making it suitable for cultivation in the first accumulated temperature zone of Heilongjiang. The mature plant height is about 97 cm without branches (Figure 2). The seeds have a brown hilum and are yellow with smooth seed coats (Figure 2). The 100-seed weight of Nongqing 28 is approximately 19.0 g. Additionally, the average contents of protein and oil in the seeds of Nongqing 28 are 38.2% and 21.2%, respectively (Table 1). In 2018 and 2019, Nongqing 28 was tested in regional trails, where the average yield of Nongqing 28 was 2593 kg/ha, resulting in a yield increase of 6.2% compared to the local cultivar Nengfeng 18 (Table 2). In 2019, Nongqing 28 was tested in the production trials, where it produced an average yield of 2660 kg/ha, increasing by 8.1% at five locations compared with the local cultivar Nengfeng 18 (Table 3). These data suggest that Nengfeng18 increased the yield, exceeding the test local soybean cultivar.

3.2. SCN Resistance of Nongqing 28

In the field assay during 2018–2022, SCN reproduction was significantly inhibited in Nongqing 28 compared to the susceptible cultivars Lee and Hefeng 50. The average numbers of cysts in Lee and Hefeng 50 were up to 69 and 67 in the 5-year field experiments, respectively (Table 3). However, the average number of cysts in Nongqing 28 was about three, with FI values ranging from 3.08 to 4.76 (FI < 10%), suggesting a resistance level close to that of the resistance control PI 437654 (Table 3). These results indicated that Nongqing 28 exhibited resistance to SCN under field conditions.
The development of SCN in Nongqing 28 was further assessed in the greenhouse (Figure 3 and Table 4). At 5 dpi, there was a significant reduction in the number of J2 in the roots of PI 437654 but not in Nongqing 28 when compared to the susceptible control soybean, Hefeng 50. However, the number of J3 in Nongqing 28 and PI 437654 was lower than in Hefeng 50 roots (Table 4). By 10 dpi, fewer J2 developed into J3/J4 in the roots of Nongqing 28 and PI 437654 compared to the number of nematodes grown to J3 or J4 in Hefeng 50 roots (Figure 3, Table 4). By 21 dpi, the average number of white females in Hefeng 50 was 51, whereas the average female numbers in Nongqing 28 was 13; almost no SCN advanced to females in PI 437654 (Table 4). Notably, the levels of plant susceptibility to SCN infection in PI 437654 was higher than in Nongqing 28. These results were consistent with the results from field tests, indicating that the development of SCN in Nongqing 28 was inhibited.

3.3. Transcription Changes in Nongqing 28 in Response to SCN Infection

To investigate the resistance mechanism of Nongqing 28, we performed RNA-seq analysis with the SCN-infected and non-infected root tissues of Nongqing 28 at 10 dpi. A total of 2808 upregulated genes and 1523 downregulated genes were identified between the infected and uninfected roots in Nongqing 28 (Figure 4A,B and Supplementary Table S1). Gene ontology (GO) enrichment analysis demonstrated that the significantly upregulated genes were involved in GO terms mainly including defence response, plant responses to biotic stimuli and oxidative stress, plant hormone-related processes, reactive oxygen species (ROS) metabolic process, regulation of protein phosphatase activity and dephosphorylation, and secondary metabolic biosynthesis such as phenylpropanoid, monocarboxylic acid, oxylipin, and flavonoid (Figure 4C). The molecular function (MF) terms affected more frequently were represented by heme binding, ADP binding, peroxidase activity, monooxygenase activity, quercetin 3-O-glucosyltransferase activity, hormone binding, and oxidoreductase activity, signaling receptor activity, and protein phosphatase activity (Supplementary Table S1). In the cell components (CCs) category, plant cell wall (GO:0009505 and GO:0005618) and external encapsulating structure (GO:0030312) were the top enriched groups (Supplementary Table S1). The KEGG analysis revealed that the most enriched terms among the upregulated DEGs were associated with phenylpropanoid biosynthesis, ABC transporters, hormone biosynthesis (Brassinosteroid and Zeatin), and secondary metabolic biosynthesis pathways such as Isoflavonoid, flavone, tropane, piperidine, pyridine alkaloid, Linoleic acid, glucosinolate, cutin, suberine, and wax (Figure 4D and Supplementary Table S1).
Furthermore, we identified key DEGs involved in soybean immune responses (Supplementary Table S2). For instance, a majority of DEGs encoding PRR proteins were upregulated in Nongqing 28 upon SCN infection, including receptor-like protein kinase (RLK), leucine-rich repeat (LRR)-RLK, lectin domain containing receptor kinase (LecRLK), serine/threonine-protein kinase (STK), receptor-like protein (RLP), and cell wall-associated receptor kinase (WAK). Of the 44 NBS-LRR-type resistance genes (NLR) which play critical roles in plant disease resistance, 41 NLR DEGs were found to be upregulated under SCN stress (Supplementary Table S2). Plant defence-related hormones ethylene (ET), jasmonic acid (JA), and salicylate acid (SA) play important roles in plant response to nematode stresses. Here, 87 DEGs involved in the biosynthesis and signaling of these three plant hormones were identified in Nongqing 28 during SCN infection. Significantly upregulated genes related to JA synthesis encoded lipoxygenases (12 DEGs), 12-oxophytodienoate reductase (1 DEG), and JA methyltransferase (4 DEGs). In the SA pathway, seven 2-oxoglutarate Fe(II)-dependent oxygenase (2OG oxygenase), three glucosyltransferase, one regulatory protein NPR1, and two MACPF domain-containing proteins exhibited upregulated expression in response to SCN infection. Among 44 DEGs encoding proteins related to ET biosynthesis and signaling in Nongqing 28, 36 DEGs were upregulated, including 1-aminocyclopropane-1-carboxylate oxidases (ACO), 1-aminocyclopropane-1-carboxylate synthases (ACS), and ethylene-responsive transcription factors (ERF) (Supplementary Table S2). In addition, other defence-related genes involved in ROS metabolic and signaling, calcium-mediating signaling, and MAPK cascades were also induced in SCN-infected roots of Nongqing 28. These proteins included respiratory burst oxidase homolog proteins (RBOH), glutathione S-transferase (GST), peroxidase, heat shock proteins (HSP), calcium-binding proteins (CaM), mitogen-activated protein kinase kinase kinases (MAPKKK), and pathogenesis-related proteins (PR), chitinase, and endo-1,3(4)-beta-glucanase (Supplementary Table S2).
To validate the results from the RNA-seq data, six upregulated DEGs related to plant defense were selected for qRT-PCR analysis in Nongqing 28 and Hefeng 50 at 10 dpi (Figure 5). These genes included GmLecRK02 (Glyma.02G221900), GmCHI03 (Glyma.03G024600), GmPR6 (Glyma.20G205700), GmWRKY40 (Glyma.14G103100), GmNIMIN1 (Glyma.10G010100), and GmLRR-RLK (Glyma.10G069500). In agreement with the RNA-seq data, all six genes, except GmNIMIN1, displayed upregulated expression in Nongqing 28 roots after SCN infection (Figure 5). In contrast, the less significant induction in the transcript levels of GmWRKY40, GmLecRK02, and GmNIMIN1 was observed in the susceptible soybean Hefeng 50 at 10 dpi. Notably, the expressions of GmCHI03, GmLRR-RLK, and GmPR6 were downregulated by SCN in Hefeng 50 roots (Figure 5).

4. Discussion

The soybean planting area in China has steadily increased due to launching China’s soybean revitalization plan policy, particularly in Heilongjiang. In 2022, the total soybean planting area reached 4.93 million ha, accounting for 47% of the total soybean harvested area in China. The occurrence of SCN has been consistently frequent and severe in soybean-producing regions of Heilongjiang. A recent survey of SCN population density and virulence phenotypes in Heilongjiang indicated that over 50% of field samples tested positive for SCN [5,15]. HG Types 0 and 7 (Race 3) are the most prevalent SCN population phenotypes in Heilongjiang [5,15]. Therefore, planting resistant soybean cultivars is a major method for controlling this pest. Recently, a series of SCN-resistant, such as KangXian, Nongqingdou, and Heinong 531, have been developed and released in the market in Heilongjiang [19,23]. However, SCN virulence changes due to the overuse of soybean cultivars with the same resistant source reported in this area [16,24,25]. Thus, it is crucial to breed new soybean cultivars with different resistance sources in Heilongjiang. In this study, we provided a novel SCN-resistant cultivar, Nongqing 28, which exhibits stable resistance to SCN Race 3 in the regional trials. Compared to the local cultivar Nengfeng 18, Nongqing 28 has high yields in both regional trials (2593 kg/ha) and production trials (average yield of 2660 kg/ha). The yield of Nongqing 28 is stably higher than the average yield of KangXian soybean cultivars (2082 kg/ha–2513 kg/ha) in Heilongjiang. Additionally, Nongqing 28 features a yellow seed coat and a brown hilum, which are more attractive in the market compared to other SCN-resistant cultivars with a less desirable black hilum [23,26]. Furthermore, Nongqing 28 has an average fat content of 21.2% in the seed, meeting the National Standards for the second-level high-oil soybean variety (≥21% fat content in seed). Its high yield potential and desirable agronomic characteristics make it a promising candidate for use as a donor in developing SCN-resistant cultivars for breeding programs.
The resistance of Nongqing 28 to SCN was further characterized in controlled greenhouse conditions. Results of acid fuchsin staining revealed that SCN development was significantly inhibited in Nongqing 28 compared to the susceptible cultivar at 10 dpi and 21 dpi. This suggested that a defense reaction occurred in the roots of Nongqing 28 in response to SCN infection and further confirmed the reliable resistance of Nongqing 28 to SCN observed in field trials, effectively suppressing the SCN lifecycle. Similarly, the inhibition of SCN development has also been found in previous research on other resistant soybean cultivars including Heinong 531, Kangxian 12, and Pendou 158 [19], and Hatiwag [27]. However, SCN infection was not affected in Nongqing 28 at an early nematode development stage (5 dpi). In comparison, a rapid and strong resistant reaction was observed in Heinong 531 at 3 dpi, which carried Peking-type SCN resistance [19]. These findings suggest that the SCN-resistant mechanism of Nongqing 28 derived from PI 437654 might differ from that of soybean cultivars with the Peking background.
Our RNA-seq data provide important information on gene expression changes to further elucidate the resistance mechanism in Nongqing 28. The most enriched GO terms and pathways mainly included plant defence response, responses to biotic stimuli, plant-pathogen interaction, secondary metabolism (phenylpropanoid and favonoid biosynthesis), hormone metabolism, ROS metabolic process, and protein phosphorylation and dephosphorylation. We observed significant upregulation of genes involved in pathogen perception and defense activation in Nongqing 28 upon SCN infection, such as RLK, STKs, NBS-LRR, WAKs and RLPs. Additionally, DEGs related to plant defense signaling, including PRs, calcium-binding protein, MAPK, RBOH, GST, peroxidase, and HSPs, were also activated in Nongqing 28. These findings suggest that an adequate recognition of the pathogen and activation of defense mechanisms may contribute to the observed resistance of Nongqing 28 to SCN. In accordance with these findings, a set of RNA-seq data showed the activation gene expression of soybean PTI and ETI components in resistant soybean cultivars in response to SCN infection [13,28,29,30,31,32]. Recent experimental evidences further supported the importance of MAPK genes (GmMAPK3 and GmMAPK6) and RLK genes (GmCDL1, GmLecRK02g, and GmLecRK08g) as the important PTI components contributing to SCN resistance through amplifying immune signaling [33,34]. The GmMAPK3/MAPK6-mediated phosphorylation of GmCDL1 activate basal immune responses and increase soybean resistance to SCN [35]. There has been some evidence for the involvement of SA, JA, and ET in soybean defense against SCN. For example, overexpression of specific genes in SA and signaling pathways, such as NPR1, TGA2, and salicylic acid methyltransferase gene SAMT, confers soybean resistance to SCN [35,36,37]. Guo et al. [38] reported that inhibition of JA signaling decreased the Rhg1a-mediated resistance to SCN. ET-insensitive soybean mutant etr1-1 exhibited enhanced host resistance to SCN infection compared to the control soybean [39]. The present work showed that the expression levels of some specific DEGs in SA, JA, and ET pathways were elevated in SCN-infected roots of Nongqing 28. Similarly, previous transcriptomic profiling revealed that many SA, JA, and ET-related genes were upregulated in other resistant soybean cultivars in the presence of SCN, suggesting that the SA, JA, and ET signaling might be the conserved defense components required for SCN resistance in soybean [28,29,30,31,32]. Therefore, SA, JA, and ET pathways may play critical role in Nongqing 28 against SCN, although this contribution did not offer a complete protection to this pest.

5. Conclusions

The present work reveals that Nongqing 28 is a new SCN-resistant soybean cultivar with high yield and favorable agronomic traits. This line can be used to enhance productivity and SCN resistance in the main soybean-producing areas of Heilongjiang. It is worth noting that rotating Nongqing 28 with other resistance resources is recommended, which may delay SCN adaptation to these SCN-resistant cultivars. Furthermore, we used RNA-seq to demonstrate that the basal defense responses were activated in SCN-infected Nongqing 28 roots. The PTI and ETI signaling components, including several RLK subfamilies, cell wall-related receptors (WAKs), ROS genes (RBOHs), and MAPK family genes, CaM genes, NBS-LRRs (ETI-associated defenses), and JAs/ET and SA signaling, might contribute to the resistance of Nongqing 28 to SCN.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14091964/s1, Table S1: List of all DEGs and Gene Ontology (GO) enrichment terms and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis of upregulated differentially expressed genes in Nongqing 28 inoculated with SCN; Table S2: List of DEGs involved in the defence-related pathways in Nongqing 28 inoculated with SCN; Table S3: List of gene primers for RT-qPCR used in this study.

Author Contributions

Conceptualization, C.Z., Y.H. (Yanfeng Hu) and J.W.; methodology, C.Z.; software, C.Z. and Y.H. (Yanfeng Hu); validation, Y.H. (Yanfeng Hu) and J.W.; formal analysis, C.Z., Y.H. (Yanfeng Hu) and J.W.; investigation, C.Z., Y.H. (Yingpeng Han), G.C., B.L., J.Y., Y.W., J.L. and L.M.; writing—original draft preparation, Y.H. (Yanfeng Hu); writing—review and editing, Y.H. (Yanfeng Hu) and J.W.; supervision, Y.H. (Yanfeng Hu) and J.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Scientific Institution Basal Research Fund of Heilongjiang province (CZKYF2023-1-B004), Leap Engineering Major Needs Science and Technology Innovation Key Program in Heilongjiang Province (CX23ZD04), Daqing Comprehensive Test Station of National Soybean Industrial Technology System (CARS-04-CES07), the Youth Innovation Promotion Association of CAS (Grant No. 2020236), and Jilin Science and Technology Department Project (20230405053RC, 2024030311NC).

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Materials. Further inquiries can be directed to the corresponding authors. Additionally, the RNA-seq raw data supporting the conclusions of this article will be made available by the authors on request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agronomy 14 01964 g001
Figure 1. Pedigree chart of soybean cultivar Nongqing 28. An 02-318 derived from Hartwig is resistant to soybean cyst nematode (SCN), but Hei 99-980 and America Xiaoheidou are susceptible to SCN.
Figure 1. Pedigree chart of soybean cultivar Nongqing 28. An 02-318 derived from Hartwig is resistant to soybean cyst nematode (SCN), but Hei 99-980 and America Xiaoheidou are susceptible to SCN.
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Agronomy 14 01964 g002
Figure 2. The phenotypes and seeds of soybean cultivar Nongqing 28 in maturity stage.
Figure 2. The phenotypes and seeds of soybean cultivar Nongqing 28 in maturity stage.
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Agronomy 14 01964 g003
Figure 3. The comparable development of soybean cyst nematode on roots of Nongqing28, PI 437654, and Hefeng 50 at 5 and 10 days post inoculation (dpi). * denotes J2, and ** denotes J3. Scale bar = 500 µm.
Figure 3. The comparable development of soybean cyst nematode on roots of Nongqing28, PI 437654, and Hefeng 50 at 5 and 10 days post inoculation (dpi). * denotes J2, and ** denotes J3. Scale bar = 500 µm.
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Figure 4. Transcriptome response of Nongqing 28 to soybean cyst nematode at 10 days post inoculation (dpi). (A) The number of differentially expressed genes (DEGs). (B) Volcano plots indicating all soybean genes of Nongqing 28 at 10 dpi. The red and green dots represent up- and downregualted genes. (C) Top 30 enriched Gene Ontology (GO) biological processes (BP) of the upregulated DEGs. (D) Top 20 most enriched KEGG terms of upregulated DEGs.
Figure 4. Transcriptome response of Nongqing 28 to soybean cyst nematode at 10 days post inoculation (dpi). (A) The number of differentially expressed genes (DEGs). (B) Volcano plots indicating all soybean genes of Nongqing 28 at 10 dpi. The red and green dots represent up- and downregualted genes. (C) Top 30 enriched Gene Ontology (GO) biological processes (BP) of the upregulated DEGs. (D) Top 20 most enriched KEGG terms of upregulated DEGs.
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Agronomy 14 01964 g005
Figure 5. Validation of DEGs in Nongqing 28 and Hefeng 50 at 10 dpi by quantity reverse transcription RT-qPCR. The expression levels of target genes are relative to the level of expression of soybean genes in the non-inoculated control plants using GmUBQ3 as reference gene. The data are presented as the means of three replicates ± SE. Asterisks indicate a statistically significant difference between soybeans genes in SCN-infected plants and the non-infected control plants (Student’s t-test, * p < 0.5).
Figure 5. Validation of DEGs in Nongqing 28 and Hefeng 50 at 10 dpi by quantity reverse transcription RT-qPCR. The expression levels of target genes are relative to the level of expression of soybean genes in the non-inoculated control plants using GmUBQ3 as reference gene. The data are presented as the means of three replicates ± SE. Asterisks indicate a statistically significant difference between soybeans genes in SCN-infected plants and the non-infected control plants (Student’s t-test, * p < 0.5).
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Table 1. Seed yield and agronomic trials of Nongqing 28 in regional tests in 2018 and 2019.
Table 1. Seed yield and agronomic trials of Nongqing 28 in regional tests in 2018 and 2019.
YearNongqing 28Nengfeng 18
Trial LocationsHeight
(cm)		Oil ContentsProtein ContentsSeed Yield
(kg/ha)		Seed Yield
(kg/ha)		Increase (%)
2018Anda Dapeng Seeds Co., Ltd.9218.9341.262471.22439.51.3
Longjiang Branch of Qishan Seeds Co., Ltd.10522.0338.412725.02565.96.2
Daqing Seeds Management Bureau9122.9737.532250.02234.40.7
Dumeng Seeds Management Bureau9021.2440.132956.72740.27.9
Tailai Seeds Station9220.7839.212426.02223.69.1
Qiqihar Branch of Heilongjiang Academy of Agricultural Sciences9119.6740.172421.22433.4−0.5
mean93.5 ± 2.320.9 ± 0.639.5 ± 0.62542 ± 103.92440 ± 80.74.1 ± 1.7
2019Anda Dapeng Seeds Co., Ltd.10722.4136.692677.92395.311.8
Qiqihar Branch of Heilongjiang Academy of Agricultural Sciences10920.1737.932623.32589.61.3
Longjiang Branch of Qishan Seeds Co., Ltd.8221.7236.432732.42388.514.4
Qinggang Experimental Station of Beifeng Seeds Co., Ltd.10922.0135.362550.02502.51.9
Tailai Seeds Station10121.6136.732521.32356.47.0
Mean101.6 ± 5.121.6 ± 0.436.6 ± 0.42621 ± 39.12446 ± 43.47.3 ± 2.6
Total97.2 ± 2.821.2 ± 0.438.2 ± 0.62593 ± 61.92443 ± 46.06.2 ± 1.5
Table 2. Seed yield of Nongqing 28 in production trials in 2019.
Table 2. Seed yield of Nongqing 28 in production trials in 2019.
Trial LocationsSeed Yield of Nongqing 28 (kg/ha)Seed Yield of Nengfeng 18 (kg/ha)Increase (%)
Anda Dapeng Seeds Co., Ltd.2523.32239.012.7
Qiqihar Branch of Heilongjiang Academy of Agricultural Sciences2663.82624.41.5
Longjiang Branch of Qishan Seeds Co., Ltd.2467.52215.011.4
Qinggang Experimental Station of Beifeng Seeds Co., Ltd.2764.42615.35.7
Tailai Seeds Station28802634.99.3
mean2660 ± 75.92466 ± 97.68.1 ± 2.0
Table 3. Reaction of Nongqing 28 to soybean cyst nematode in fields during 2018–2022.
Table 3. Reaction of Nongqing 28 to soybean cyst nematode in fields during 2018–2022.
Soybean
Cultivars		20182019202020212022
Cysts aFI (%) bCysts aFI (%) bCysts aFI (%) bCysts aFI (%) bCysts aFI (%) b
Lee63 ± 4.15 A10065 ± 5.57 A10069 ± 4.74 A10068 ± 6.53 A10053 ± 5.52 A100
Hefeng 5047 ± 2.55 A74.6052 ± 4.16 A80.0067 ± 4.06 A97.158 ± 3.90 A85.2951 ± 4.90 A96.2
Nongqing 283 ± 0.42 B4.762 ± 0.43 B3.083 ± 0.50 B4.353 ± 0.46 B4.412 ± 0.49 B3.57
PI 4376541 ± 0.33 B1.592 ± 0.60 B3.081 ± 0.42 B1.452 ± 0.72 B2.941 ± 0.52 B1.89
a Data are mean ± SE of 20 replicates. Uppercase letters represent significant difference at level of p < 0.05 by statistical analysis. b FI = (average number of females on the soybean cultivar/average number of females on the susceptible check of Lee) × 100.
Table 4. Comparison of soybean cyst nematode development in Nongqing 28 and Heifeng 50.
Table 4. Comparison of soybean cyst nematode development in Nongqing 28 and Heifeng 50.
Soybean Cultivars5 dpi10 dpi21 dpi
J2J3J2J3J4Female
Hefeng 50205 ± 8.14 a18 ± 3.21 a107 ± 8.77 a73 ± 3.31 a5 ± 0.53 a51 ± 5.93 a
Nongqing 28193 ± 6.51 a12 ± 1.53 b95 ± 9.69 a41 ± 3.01 b2 ± 0.43 a13 ± 1.73 b
PI 437654165 ± 4.84 b3 ± 0.88 c83 ± 4.67 a23 ± 2.92 c0 ± 0 b0 ± 0.10 c
Data are mean ± SE. Different letters represent significant difference at level of p < 0.05 by statistical analysis. dpi, days post inoculation; J2, second-stage juveniles; J3, third-stage juveniles; J4, fourth-stage juveniles.
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Zhou, C.; Hu, Y.; Han, Y.; Chen, G.; Liu, B.; Yu, J.; Wu, Y.; Li, J.; Ma, L.; Wei, J. Resistance Analysis of a Soybean Cultivar, Nongqing 28 against Soybean Cyst Nematode, Heterodera glycines Ichinohe 1952. Agronomy 2024, 14, 1964. https://doi.org/10.3390/agronomy14091964

AMA Style

Zhou C, Hu Y, Han Y, Chen G, Liu B, Yu J, Wu Y, Li J, Ma L, Wei J. Resistance Analysis of a Soybean Cultivar, Nongqing 28 against Soybean Cyst Nematode, Heterodera glycines Ichinohe 1952. Agronomy. 2024; 14(9):1964. https://doi.org/10.3390/agronomy14091964

Chicago/Turabian Style

Zhou, Changjun, Yanfeng Hu, Yingpeng Han, Gang Chen, Bing Liu, Jidong Yu, Yaokun Wu, Jianying Li, Lan Ma, and Jian Wei. 2024. "Resistance Analysis of a Soybean Cultivar, Nongqing 28 against Soybean Cyst Nematode, Heterodera glycines Ichinohe 1952" Agronomy 14, no. 9: 1964. https://doi.org/10.3390/agronomy14091964

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