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Zhao, R.; Kang, I.; Lee, S. Xanthomonas citri pv. glycines in Soybean. Encyclopedia. Available online: https://encyclopedia.pub/entry/41580 (accessed on 17 May 2024).
Zhao R, Kang I, Lee S. Xanthomonas citri pv. glycines in Soybean. Encyclopedia. Available at: https://encyclopedia.pub/entry/41580. Accessed May 17, 2024.
Zhao, Ruihua, In-Jeong Kang, Sungwoo Lee. "Xanthomonas citri pv. glycines in Soybean" Encyclopedia, https://encyclopedia.pub/entry/41580 (accessed May 17, 2024).
Zhao, R., Kang, I., & Lee, S. (2023, February 23). Xanthomonas citri pv. glycines in Soybean. In Encyclopedia. https://encyclopedia.pub/entry/41580
Zhao, Ruihua, et al. "Xanthomonas citri pv. glycines in Soybean." Encyclopedia. Web. 23 February, 2023.
Xanthomonas citri pv. glycines in Soybean
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This entry is adapted from the peer-reviewed paper 10.3390/agronomy13020490

Soybean [Glycine max (L.) Merr.] is an economically important crop with high protein and oil contents. A range of biotic stresses constantly threaten soybean production and lead to decreases in yield and quality, bacterial pustule caused by Xanthomonas citri pv. glycines (Xcg) is one of the most destructive diseases affecting worldwide soybean production.

soybean bacterial pustule diversity of Xanthomonas citri pv. glycines (Xcg)

1. Introduction

Soybean [Glycine max (L.) Merr.] is the most economically important legume crop and provides edible oil and protein used in food, feed, and industrial products worldwide [1][2][3]. The percentages of oil and protein in soybean seeds are almost 18.0% and 38.0%, respectively [4]. As estimated, almost 40.0% of the edible vegetable oil consumed worldwide is produced from soybeans [5]. Unfortunately, soybean is susceptible to numerous pests and pathogens, including aphids, beetles, mites, stinkbugs, nematodes, viruses, bacteria, oomycetes, and fungi, resulting in decreased yield and quality [6][7][8]. For example, the cumulative economic loss from 1996 to 2016 due to 23 diseases across 28 states in the United States was $73,535 per hectare [9]. These 23 diseases can be grouped into six categories: stem/root, nematode, foliar, bacteria, virus, and other diseases. Of these, infection with bacterial diseases specifically results in a $529 per hectare loss at the national level (across 28 states and 21 years) [9].
Bacterial pustule (BP) caused by Xanthomonas citri pv. glycines (Xcg) is one of the most significant bacterial diseases in susceptible soybean genotypes worldwide [10]. Over the last 120 years, the identification and distribution of Xcg has been continuously documented around the world [11][12][13][14][15][16][17][18]. Several genetic studies have identified genomic regions associated with resistance to Xcg using mapping populations and collections of soybean accessions [10][19][20][21][22][23][24][25][26][27], with a 33-kb region located on chromosome 17 often identified as a strong candidate locus [20]. Molecular markers associated with resistance to Xcg have also been reported in a few studies. Genome-wide gene expression was compared between soybean near-isogenic lines carrying either a BP-resistant or -susceptible allele following inoculation with Xcg [28]. However, resistance genes for Xcg have yet to be cloned, and much remains unknown despite these efforts. Recent research has revealed that the genetic diversity of BP isolates is increasing, and molecular evidence suggests that a population shift has occurred in Xcg during the past 20 years [13][16][29]. Climate change also increases the possibility of changes in the Xcg population, but little work has been done in the past decade to mine new genetic sources and identify resistance genes/quantitative trait loci (QTLs).

2. Bacterial Pustule and Its Causal Agent Xanthomonas citri pv. glycines

Xanthomonas citri pv. glycines (Xcg) is the causal agent of BP [30]. Hedges [31] first identified the typical pustule symptoms caused by this disease and named the causal agent Bacterium phaseoli var. sojense. The pathogen was later reclassified to Xanthomonas campestris pv. glycines [32] and then Xanthomonas axonopodis pv. glycines through DNA–DNA hybridization analysis [33] before finally receiving the name Xanthomonas citri pv. glycines [30].
Xcg is a Gram-negative, aerobic, and motile bacterium with a single polar flagellum. It is rod shaped, with sizes of 0.5–0.9 μm (width) × 1.4–2.3 μm (length). This bacterium can grow at 10–40 °C (but grows optimally at 30–33 °C in wet conditions) and at a pH of 4.0–8.0 (optimal pH = 7.0). Colonies on tryptic soy agar are small, circular, and smooth, and have entire margins. The bacterium grows slowly in culture and is known to produce auxins, cytokinin, bacteriocins, toxins, and extracellular polysaccharides, among other molecules [34][35][36][37].
Several molecular biology tools and techniques, including polymerase chain reaction (PCR) and real-time quantitative PCR (qPCR), have been used to detect Xcg directly in plant tissues and seeds. Primers for DNA hybridization and conventional PCR have been developed for the glycinecin A (glyA) gene [38][39] and the PstI fragment containing the open reading frame of the TAL gene [40]. Real-time PCR methods based on the rpoD gene can also detect the presence of Xcg and quantify the degree of Xcg contamination in seeds [41].
DNA sequences of various genes have been utilized to analyze the genetic relatedness of different species within the genus Xanthomonas, as well as that of different strains within the species X. citri. According to Constantin et al. [30], a gyrB fragment was selected as an effective target gene for the identification of Xanthomonas taxa [42].
For differentiation within Xanthomonas species, multi-locus sequence analysis (MLSA) has been used in phylogenetic analysis, and recently, 109 Xanthomonas strains were distinguished based on seven housekeeping genes (atpD, dnaK, efp, glnA, gyrB, rpoD, lepA, and lrp) [30][43]. These analyses showed that Xcg is closely related to some pathogenic bacterial species on different hosts, namely X. axonopodis pv. citri and X. citri pv. mangiferaeindicae, but it is relatively distant from X. campestris pv. syngonii and X. axonopodis pv. axonopodis [30].
Key symptoms of BP, shown in Figure 1, include small, yellowish spots that later turn reddish-brown and slightly raised pustules in the center of the lesions [44]. The pustules often arise through hypertrophic changes in the parenchymatous tissues of the host responding to the bacterial infection. Pustule production on soybean leaves is known to be accompanied by a drastic increase in indole-3-acetic acid content in host tissues [45]. These lesions often occur on the abaxial side of leaves and vary from specks to large, irregularly shaped, and mottled-brown areas, which develop when the lesions coalesce. The leaf spots can form without developing pustules.
Agronomy 13 00490 g001
Figure 1. Bacterial pustule symptom caused by Xanthomonas citri pv. glycines on a susceptible soybean genotype.
The etiology of BP is fairly well understood. Xcg can infect common bean and cowpea as well as soybean [46]. It overwinters in seeds, on plant debris in the soil, and in the soil itself. Xcg enters the plant through natural openings and wounds, where it multiplies intercellularly. Xcg invades and multiplies within the apoplast, causing localized leaf spots or leaf streaks [47]. Plant-to-seed infection occurs via the vascular system through the funiculus as well as through infected pods. Seeds can also get contaminated with the bacterium during threshing after harvest. Infections are more common on younger leaves, which are more susceptible than older leaves, although the disease appears at all stages of plant growth [22][48][49]. Disease incidence depends on the susceptibility of the soybean genotype, virulence of the pathogen, and favorability of weather conditions. Bacterial cells are spread by wind-blown rain, by rain splashing up from old crop residue, and during field work when the canopy is wet. For the disease to occur, soil- and seed-borne inocula must be spread during warm and humid weather, which promotes fast multiplication of the bacterium. Kang et al. [29] reported that disease severity of BP in Korea is often correlated with the amount of precipitation in August when soybean plants are at the flowering stage. Thus, especially wet conditions are likely to be one of the main factors contributing to a high incidence of BP.

3. Distribution and Population Diversity of Xcg

Xcg is widely distributed and commonly occurs in major soybean-producing countries such as Brazil, the United States, China, Korea, Thailand, Australia, and Benin [50]. In recent years, disease severities of up to 26% and incidences of up to 70% have been reported in several countries [18][51]. In addition, the bacterium was reported to be present in areas where it had not previously been found. For instance, in the United States, the disease had commonly been found in the southern region, but more recently it was also reported as far north as North Dakota [15]. In China, the disease is most severe in South China, especially in the Yangtze and Huai River Basins. The incidence of BP has been increasing due to global warming and the more frequent occurrence of storms [16][52]. It was also reported that BP occurred during all four seasons in the northern coastal region of New South Wales, Australia [53]. In Benin, Africa, BP was present in 33 of 34 sites in the Guinea Savanna, with mean incidence varying from 15 to 70% [18]. In Korea, BP occurs nationwide and can be observed from July to September. During the 1990s and 2000s, BP was so severe that it could be observed in 86–89% of all soybean fields in Korea [54].
Strains of the BP pathogen have been shown to fall into distinct races [29][42][55][56] that differ in aggressiveness [57]. Hwang et al. [42] evaluated the pathogenic variability of 63 Xcg isolates in a set of 11 differential soybean cultivars, including Chippewa, Harosoy, Mukden, Pella, and Williams. Based on the results of this experiment, they classified the isolates into five races, designated 1, 2, 3, 4, and 5. Similarly, Kaewnum et al. [57] demonstrated that 26 Xcg isolates from Thailand differed in their capability to induce disease on soybean cultivars and in their ability to induce a hypersensitive response (HR) in a range of plant species, including tobacco (Nicotiana tabacum), cucumber (Cucumis sativus), pea (Pisum sativum), and sesame (Sesamum indicum). They classified these Thai Xcg isolates into three races based on the presence of an avr gene that contributes to differential virulence on soybean cultivars. Park et al. [56] classified 155 Xcg isolates from Korea into six groups based on the number and size of genomic fragments hybridizing with an avrBs3 gene family probe, as differences in avrBs3 content are correlated with resistance and/or aggressiveness. They also identified six type strains that represent these groups. As a follow-up to that study, Kang et al. [29] characterized the diversity of a nationwide collection of 106 Korean Xcg isolates based on avrBs3 banding patterns and reported that the diversity of Xcg strains increased during the last two decades. They also documented the emergence of new type strains along with new dominant strains.

4. Molecular Mechanisms Underlying Bacterial Pustule Formation in Soybean

During disease establishment, Xanthomonas pathogens such as Xcg employ various virulence factors, including adhesins, polysaccharides, lipopolysaccharides, and degradative enzymes. One key pathogenicity factor is the type III secretion system (T3SS), which enables bacteria to directly inject effector proteins into the host cell cytosol. The type III (T3) effectors are translocated into the host cells, where they interfere with host immunity responses or facilitate the nutritional or virulence processes of the pathogen [47][58][59]. The T3SS is encoded by the hypersensitive reaction and pathogenicity (hrp), hrp-conserved (hrc), and avirulence (avr) genes and reacts with specific resistance (R) receptors. Effector proteins are encoded by hrp-dependent out protein (hop) genes [60].
Kim et al. [61] characterized the HrpT3SS and hpa (hrp-associated) virulence genes and identified HR-eliciting proteins such as HpaG in the Xcg genome. The pathogenicity island (PAI) contained seven plant-inducible promoter boxes and was composed of nine hrp, nine hrc, and eight hpa genes that are regulated by HrpG and HrpX. The Hrp PAI in Xcg resembled that of other Xanthomonas species, and the Hrp PAI core region was highly conserved.
The largest effector family found in the Xanthomonas spp. is the AvrBs3/PthA or TAL family. Xanthomonas strains express a combination of typically 20–40 T3 effectors. Xcg strains possess more than 30 T3 effectors and contain at least four homologs of avrBs3. It was reported that Korean Xcg strains display the greatest variation in avrBs3 homolog numbers, and their plasmids also carry several avrBs3 homologs [13]. According to Athinuwat et al. [55], the avrBs3 homolog avrXg1 contributes to increased bacterial establishment in soybean leaves and acts as a determinant for virulence specificity. Similarly, several TAL effectors from Xanthomonas oryzae pv. oryzae (Xoo) are essential virulence factors for the infection of rice (Oryza sativa) [47]. Meanwhile, a variety of transcription activator-like (TAL) effectors are known to be associated with pathogen virulence and disease symptoms, and the presence or absence of specific effectors can contribute to the pathogenicity on specific hosts [62]. The specificity of TAL effectors is determined by repeat-variable diresidues (RVDs), which allow binding to the promoter of the host plant [63]. Recently, whole-genome sequencing of Xcg strains revealed that the diversity and size of RVDs are limited within Xcg, and also predicted that the effector binding elements of the TAL effectors fall into six groups and are strongly overlapping in sequence [11]. This suggests that the target binding domains in soybean cultivars may evolve specifically. However, despite these studies, little is known about the corresponding host virulence targets of TAL effectors and their role in pathogenicity.
Previous research has identified candidate genes in soybean that relate to BP resistance (Table 1) [10][19][25][26][64][65]. Gene-encoding membrane proteins, zinc finger family proteins, LRR-RLK resistance proteins, Benzyl alcohol O-benzoyl transferase-like protein, MAIN-LIKE 1-like protein, Lateral organ boundaries (LOB), CASP-like protein 4A3, E3 ubiquitin-protein ligase SIS3-like, LATERAL ORGAN BOUNDARY1 and a defective hydroperoxide lyase (HPL) gene, among others, are related to BP resistance. The control of BP is complicated because many small QTLs influence plant resistance. However, soybean breeders could adopt gene cloning using the genes implicated in the disease resistance.
Table 1. Candidate genes for resistance to Xcg in the previous studies.
  Reference Chr.
(LG) a		 Gene ID Position b Functional Annotation
1 Kim et al. 2010 [20] 17 (D2) Glyma.17g090100 7,020,522…7,022,065 Membrane protein At2g36330; Arabidopsis thaliana
    17 (D2) Glyma.17g090200 7,028,352…7,034,934 Zinc finger (C3HC4-type RING finger) family protein; Arabidopsis thaliana
2 Chang et al. 2016 [26] 1 (D1a) Glyma.01g197600 53,149,380…53,153,676 LRR-RLK resistance gene
    1 (D1a) Glyma.01g197800 53,170,021…53,173,875 LRR-RLK resistance gene
    11 (B1) Glyma.11g196800 27,106,029…27,107,951 LRR-RLK gene
    17 (D2) Glyma.17g090400 7,040,797…7,042,768 RLK gene
3 Zhang et al. 2018 [66] 2 (D1b) Glyma.02g108700 10,404,064…10,404,874 Calcium-binding EF-hand family protein
    2 (D1b) Glyma.02g110500 10,655,319…10,660,151 NB-ARC domain-containing disease resistance protein
    2 (D1b) Glyma.02g112300 10,900,201…10,902,765 NB-ARC domain-containing disease resistance protein
    2 (D1b) Glyma.02g120800 11,926,840…11,931,251 Leucine-rich repeat receptor-like protein kinase family protein
    17 (D2) Glyma.17g204600 33,223,552…33,226,195 Receptor-like protein 12
    17 (D2) Glyma.17g204300 33,083,927…33,090,560 Enhancer of polycomb-like transcription factor protein
    19 (L) Glyma.19g074900 27,195,325…27,202,148 LRR protein kinase family protein
4 Capobiango da Fonseca et al. 2021 [19] 3 (N) - - Benzyl alcohol O-benzoyl transferase-like (LOC100793892)
  15 (E) - - Protein MAIN-LIKE 1-like (LOC102667247)
5 Wang et al. 2020 [25] 12 (H) Glyma.12g191400 35,295,823…35,301,648 Defective hydroperoxide lyase (HPL) gene
6 Zhao et al. 2022 [10] 5 (A1) Glyma.05g040500 3,625,982…3,628,389 LBD domain-containing transcription factor
    17 (D2) Glyma.17g086300 6,660,761…6,663,277 Lateral organ boundaries (LOB) domain-containing protein 25
    17 (D2) Glyma.17g090100 7,020,522…7,022,065 CASP-like protein 4A3
    17 (D2) Glyma.17g090200 7,028,352…7,034,934 E3 ubiquitin-protein ligase SIS3-like
    17 (D2) Glyma.17g090400 7,040,797…7,042,768 Uncharacterized

a Chr., Chromosome; LG, Linkage group. b Physical positions (in base pairs) are based on the reference genome Glyma.Wm82.a2 (Glyma2).

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Subjects: Agronomy
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Ruihua Zhao
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In-Jeong Kang
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Sungwoo Lee
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Update Date: 23 Feb 2023
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