Impact of bacterial leaf blight disease ( Pantoea agglomerans ) on forage yield and feeding value of oat

doi:10.21203/rs.3.rs-3774754/v1

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Impact of bacterial leaf blight disease ( Pantoea agglomerans ) on forage yield and feeding value of oat

https://doi.org/10.21203/rs.3.rs-3774754/v1

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From 2018 to 2019, bacterial leaf blight disease (LBD) caused by Pantoea agglomerans was observed on the leaves of oat (Avena sativa L.) in Northwest China, and diseased oat often showed yellow-colored necrotic symptoms on the leaves. This is a new bacterial disease of oat in China. In this study, greenhouse experiments were conducted to explore the effect of LBD (P. agglomerans) on forage yield and feeding value of Avena sativa [Baiyan 2 (B2)] and A. nuda [Baiyan 7 (B7)]. The results revealed that effective tillers, plant height, flag-leaf length, flag-leaf width, fresh weight, dry weight, fresh-dry ratio, crude ash, crude protein, ether extract, soluble carbohydrate, calcium, phosphorus, digestible dry matter, dry matter intake and relative feed value of B2 and B7 were all significantly (P < 0.05) decreased by LBD. Hay yield of oat was reduced 1.38 to 23.48%, and relative feed value was decreased 1.01 to 26.24% by LBD. In contrast, crude fiber, acid detergent fiber, neutral detergent fiber and nitrogen free extract of B2 and B7 were significantly (P < 0.05) increased after inoculation of P. agglomerans. Moreover, B7 had a higher forage yield and relative feed value than B2 under inoculation and non-inoculation of P. agglomerans. LBD (P. agglomerans) has negative influences on growth, forage yield and feeding value of oat, and these negative effects are enhanced with increase of LBD severity.

Pantoea agglomerans

leaf blight disease

oat

plant growth

forage yield

nutritional quality

Oat (Avena sativa L.) is the most cropped cereal and fodder crop in the word, and it is ranked sixth after wheat, maize, rice, barley and sorghum, and mainly cultivated as a major spring crop in arid and semiarid regions of the world, such as Northern Europe, North America, Australia, Canada and China (Antonia et al., 2011; Boczkowska et al., 2013; Marshall et al., 2013; Yang et al., 2023). It is a major food source for human consumption, livestock feed providing valuable nutrients, and has usually been considered to be an excellent forage due to its high-forage yield, high nutritional value, lower neutral washing fiber content and good palatability (Havrlentova et al., 2013; Kumar et al., 2017; Sadras et al., 2019). Furthermore, oat has an excellent growth habit, strong abiotic stress resistance and lower summer heat requirements or input than other cereal crops (Havrlentova et al., 2013; Allwood et al., 2019). Thus, high yield and good quality of oat production has an economic and social importance for human food security and livestock nutrition.

Oat crops generally suffer from fungal, bacterial and viral diseases, and diseases are one of the most important factors limiting oat performance and yield in many oat growing areas of the world (Larijani et al., 2019). The diseases of oat, include smut (Ustilago spp.)(Menzies et al., 2009), red leaf (Barley yellow dwarf virus, BYDV) (Robertson & French, 2007), powdery mildew (Blumeria graminis)(Sylwia & Kowalczyk, 2012), Fusarium head blight (Fusarium spp.)(Tekle et al., 2013), leaf spot (Pyrenophora avenae/Bipolaris spp.)(Soovli et al., 2010; Aggarwal et al., 2011), bacterial leaf blight (Pseudomonas spp.)(Ishiyama et al., 2013), crown rust (Puccinia coronata)(Carson, 2009) and stem rust (Puccinia graminis)(Gnocato et al., 2018), which occur in most oat producing areas of oats worldwide. The occurrence and development of these diseases can not only hinder growth and productivity of oat, but also can reduce the economic and nutritional value of forage and grain (Li et al., 2017; Dietz et al., 2019).

P. agglomerans is a Gram-negative bacterium in the family of Enterobacteriaceae, which occurs frequently in agricultural and natural environments, such as plants, seeds, water, soil, humans and animals (Dutkiewicz et al., 2015; José et al., 2018). This species is usually known as an epiphytic or endophytic bacterium developing in a variety of plants, and can not only promote plant growth, but also control plant diseases based on its biocontrol ability against some plant pathogens (e.g, Pseudomonas marginalis, Xanthomonas retroflexus, Erwinia amylovora and Penicillium digitatum, etc.) (Zamani et al., 2009; Omer et al., 2010; Kim et al., 2012; Quecine et al., 2012; Sadik et al., 2015). On the other hand, this bacterium is an emerging pathogen causing infections of soft tissues, bone and joints in humans, and can result in ventilator associated pneumonia, as well as primary or catheter related bacteremia (Cruz et al., 2007; Saha et al., 2015; José et al., 2018). Furthermore, P. agglomerans can also cause leaf spots, blights and rot diseases on many plants as a plant pathogen, including top or stem rot on maize (Yao et al., 2019), boll rot of cotton (Medrano & Bell, 2010), leaf spot on Araceae family (Yazdani et al., 2018), and leaf blight diseases (LBD) of onions (Edens et al., 2006), rice (Lee et al., 2010), walnuts (Wang et al., 2016), pepino melon (She et al., 2021) and maize and sorghum (Morales et al., 2007). From 2018, leaf blight disease (LBD) caused by P. agglomerans occurred in large oat planting areas of Huan county Qingyang City, Gansu Province in northwestern China. This was the first report of P. agglomerans causing LBD on oat (Wang et al., 2022a).

Our previous study has found that LBD (P. agglomerans) can decrease seed germination, seedling growth and photosynthetic efficiency of oat (Wang et al., 2022b and c), but the effects of LBD incited by P. agglomerans on forage yield and feed quality of oat (A. sativa and A. nuda) is unknown. Therefore, we wanted to determine the impacts of P. agglomerans on forage yield and feeding value of covered and naked oat (A. sativa and A. nuda). We hypothesized that 1) P. agglomerans negatively affects the forage yield and feeding value of oat, 2) the effects of P. agglomerans on covered and naked oat plants differ because of different plant biology, and 3) these effects are increased with the development of LBD.

2.1 Plant materials

The two common oat varieties: “Baiyan 2” (B2) and “Baiyan 7” (B7), were used in this study. Both are widely planted in northern China. The seeds of A. sativa (B7) and A. nuda (B2) were all obtained from Baicheng City, Jilin Province of China (45°37' N, 122°48' E, Altitude 155 m) in 2018, respectively. The well-filled, healthy-looking seeds were collected in sterilized polythene bags and stored at a constant 4°C at the Lanzhou Official Herbage and Turfgrass Seed Testing Centre, Ministry of Agriculture, Lanzhou, China for further investigation.

2.2 Bacterial suspension preparation

Isolation and identification of pathogenic bacteria LBD on oat leaves were done in a previous study (Wang et al., 2022a). Pure strains of P. agglomerans grown on nutrient agar (NA) in dark conditions for 24 to 48 h at 25°C were suspended in sterile distilled water to obtain approximately 10⁸ (CFU)/mL by optical density readings with Biolog turbidimeter (Biolog Inc., Hayward, USA). The prepared bacterial suspensions were used for inoculation.

2.3 Seed treatment and seedling cultivation

On October 18, 2021, B2 and B7 seeds were separately surface sterilized with 1% NaOCl solution for 10 min, 75% ethanol for 5 min, followed by washing with sterile water 5 times and dried with sterile filter paper. The sterilized seeds were planted in 48 hole plastic seedling trays containing sterilized vermiculite, and after seedlings grew two leaves, they were transplanted into plastic pots (20 cm diameter, 30 cm height) containing the same amount of sterilized media (forest brown soil and natural soil in a w/w ratio 1:2). The natural soil was collected from an experimental field at Lanzhou University. Each pot had only one seedling and an equal initial water content. All pots were randomly placed in a constant temperature greenhouse (temperature 22 ± 2°C, humidity 42 ± 2%) at the College of Pastoral Agriculture Science and Technology, Lanzhou University, and irrigated equally daily.

2.4 Bacterium inoculation

Three-week-old healthy oat seedlings in greenhouse with same growth status were selected for inoculation with bacterial suspension onto leaves using needleless syringe injection inoculation method (suspensions infiltrated into leaf tissues) (Azad et al., 2000). Oats inoculated with sterile distilled water were used as controls (CK). A total of 180 potted plants were used for inoculating bacterial suspensions and water. All inoculated seedlings were placed in transparent polyethylene bags and moistened with sterile distilled water until the first symptoms started to occur. All plants were maintained in a greenhouse and observed daily for three weeks for the development of symptoms. Re-isolation of bacteria from inoculated plant lesions of leaves were done and determined to be P. agglomerans by colony morphology on NA and physiological and biochemical tests.

2.5 Disease rating

The average disease infection rate (ADR) and average disease index (ADI) were separately recorded 5 times in jointing, flowering and milking stages of oat. LBD (P. agglomerans) disease rating criteria were based on the system of bacterial LBD in rice (Sania et al., 2015; Ashfaq et al., 2016) (Table 1). Our experiment involved 6 disease ratings × 2 oat varieties × 15 replicates per disease rating, resulting in a total of 180 potted plants used.

Table 1

Disease rating criteria of bacterial LBD in rice.
Disease rating	Rating criteria
grade 0	Asymptomatic
grade 1	Lesion length 2–3 cm
grade 2	Lesion length less than 1 / 4 of leaf length
grade 3	Lesion length more than 1 / 4 of leaf length, but less than 1 / 2
grade 4	Lesion length more than 1 / 2 of leaf length, but less than 3 / 4
grade 5	Lesion length less than 3 / 4 of leaf length

2.6 Measurement parameters

After calculating ADR and ADI, all plants included in this study were used to measure the parameters of forage yield and nutritional quality at milking stage, respectively. The effective tillers (ET), plant height (PH), flag-leaf length (FLL) and flag-leaf width (FLW) were determined, and all plants were cut to 1 cm above ground and separated into stem and foliage components and the fresh weight (FW) of stem and leaf were recorded. Dry weight (DW) was obtained after oven-drying the tissue at 80°C until a constant weight was reached, and fresh-dry ratio (FDR) and stem-leaf ratio (SLR) were calculated. Crude ash (CA) was measured after igniting 2 g of samples in a muffle furnace (Gallenkamp, Loughborough, UK) at 550°C overnight and the results were expressed as a percentage of the initial weight of samples (Jayawickrama et al., 2013). Crude protein (CP) was obtained by total N determination using a Kjeldahl apparatus and the results were calculated by fixed conversion factor (Chizzotti et al., 2009; Muhammad et al., 2017). Ether extract (EE) percent was estimated by the petroleum ether extraction method using Soxhlet Extraction System (Chen et al., 2015). Crude fiber (CF), acid detergent fiber (ADF), neutral detergent fiber (NDF) and nitrogen free extract (NFE) were determined and calculated by the methods of Chizzotti et al. (2009) and Muhammad et al. (2017). Soluble carbohydrate (SC) was measured by the anthrone method (John et al., 2010). Calcium and phosphorus were assayed by graphite furnace atomic absorption spectrometry and phosphorus vanadium molybdate yellow colorimetric method, separately (Li, 2007). Digestible dry matter (DDM), dry matter intake (DMI) and relative feed value (RFV) were calculated by the formula in Basbag (2021) and Lamidi et al. (2021). Disease ratings were randomly done by selecting 5 points from leaves of each plant, and it was repeated 5 times. Experiments were repeated 2 times.

2.7 Statistical analysis

Data analyses were performed with SPSS 19.0 (SPSS, Inc., Chicago, IL, U.S.A.) to analyze the effects of oat varieties and P. agglomerans on ET, PH, FLL, FLW, FW, DW, FDR, SLR, CA, CP, EE, CF, ADF, NDF, NFE, SC, calcium, phosphorus, DDM, DMI and RFV of B7 and B2. A two-way ANOVA was performed, and a repeated-measures ANOVA with Fishers Least Significant Differences (LSD) test was used to determine whether differences between means were statistically significant. Statistical significance was defined at the 95% confidence level and means were reported with their standard errors.

Structural equation modeling (SEM) was used to describe the potential causal relationships between explanatory variables, forage yield and feeding value. SEM analysis was performed with IBM SPSS Amos 24.0 (Amos Development Co., Greene, Maine, U.S.A.). The strength of direct and indirect relationships in different variables and areas was calculated based on the results of linear regression. The SEM models based on the potential relationships and known factors among the drivers of forage yield and feeding value were constructed, and a step-wise fitting procedure was used to achieve the best-supported model based on GFI (Goodness of Fit Index), SRMR (Standardized Root Mean square Residual) and RMSEA (Root Mean Square Error of Approximation).

3.1 ADR and ADI of oat in jointing, flowering and milking stages

The ADR and ADI of B2 and B7 were different in jointing, flowering and milking stages of oat. After inoculating P. agglomerans in the seedling stage, ADR and ADI of LBD in B2 and B7 were significantly (P < 0.05) increased with oat phenological development. Moreover, these parameters were also influenced by oat varieties, ADR and ADI of B7 were significantly (P < 0.05) higher than in B2 in all growth stages (Table 2).

Table 2

Average disease infection rate (ADR) and average disease index (ADI) of LBD in B2 and B7 in jointing, flowering and milking stages.
Indices	Varieties	Growth stages
Indices	Varieties	Jointing	Flowering	Milking
ADR (%)	B2	72.31 ± 0.84a*	78.46 ± 0.67b*	84.82 ± 1.17c*
ADR (%)	B7	78.92 ± 1.35a	85.33 ± 1.54b	93.16 ± 2.48c
ADI	B2	43.52 ± 2.11a*	48.77 ± 0.94b*	51.83 ± 1.57c*
ADI	B7	48.75 ± 1.19a	56.49 ± 1.85b	68.35 ± 0.81c
Different lowercase letters stand for significant (P < 0.05) differences in different growth stages, * is significant (P < 0.05) in different varieties.

3.2 Effects of LBD (P. agglomerans) on the parameters of plant growth

Effective tillers (ET), plant height (PH), flag-leaf length (FLL) and width (FLW) of B2 and B7 were negatively affected by LBD. P. agglomerans infection caused a significant (P < 0.05) decrease in these growth parameters of B2 and B7 with the disease rating increasing from 0 to 5 (Fig. 1). Comparing with healthy plants, ET, PH, FLL and FLW of diseased oat were reduced by 40.72%, 14.3%, 11.93% and 12.72% on average, respectively. The changes of these parameters between B2 and B7 were also different. ET, FLL and FLW of B7 were greater than that of B2 in healthy and diseased conditions (Fig. 1A, C and D), but PH of B7 was less than B2 with disease rating increasing from 0 to 5 (Fig. 1B). Oat varieties (V) and LBD (D) had significant (P < 0.05) influences on ET, PH, FLL and FLW of oat, and the interaction effects of “V×D” were also significant (P < 0.05) (Table 3).

Table 3

Results of two-way ANOVA for the effects of varieties (V) and disease (D) on effective tillers, plant height, flag-leaf length and width of oat.
Source	df	Effective tillers		Plant height		Flag-leaf length		Flag-leaf width
Source	df	F-value	P	F-value	P	F-value	P	F-value	P
V	1	15.464	<0.001	204.410	<0.001	172.841	<0.001	12.049	0.002
D	5	34.997	<0.001	255.529	<0.001	360.694	<0.001	23.611	<0.001
V×D	5	4.075	<0.001	7.381	<0.001	3.562	0.004	3.099	0.010

3.3 Effects of LBD (P. agglomerans) on the parameters of forage yield

LBD had significantly (P < 0.05) negative effects on fresh weight (FW), dry weight (DW), fresh-dry ratio (FDR) and stem-leaf ratio (SLR) of B2 and B7. As the increasing of disease rating, FW, DW and FDR of B2 and B7 were significantly (P < 0.05) decreased, but SLR was significantly (P < 0.05) increased (Table 4). The average FW and DW of diseased oat were reduced by 11.3% and 9.7% respectively compared with that of healthy oat. Furthermore, FW, DW and FDR of B7 were greater than B2, but SLR in B7 was less than it in B2 (Table 4). Oat varieties (V) and LBD (D) had significant (P < 0.05) effects on FW, DW, FDR and SLR of oat, while their interaction of “V×D” on these parameters was not evident (Table 5).

Table 4

Fresh weight, dry weight, fresh-dry ratio and stem-leaf ratio of B2 and B7 under 6 disease ratings.
Index	Varieties	Disease rating
Index	Varieties	0	1	2	3	4	5
Fresh weight (g)	B2	48.31 ± 1.56a	48.13 ± 0.72a	46.39 ± 1.29b	44.25 ± 0.57c	40.19 ± 0.32d	37.63 ± 0.84e
Fresh weight (g)	B7	54.96 ± 1.25a	53.65 ± 1.15ab	51.93 ± 0.49b	49.55 ± 0.84c	45.79 ± 0.65d	41.30 ± 0.23e
Dry weight (g)	B2	18.40 ± 0.32a	18.33 ± 0.44a	18.00 ± 0.18ab	17.83 ± 0.27b	16.66 ± 0.55c	15.86 ± 0.39d
Dry weight (g)	B7	18.72 ± 0.53a	18.68 ± 0.27a	18.37 ± 0.58ab	18.23 ± 0.42b	17.04 ± 0.16c	16.09 ± 0.31d
Fresh-dry ratio	B2	2.63 ± 0.07a	2.62 ± 0.08a	2.57 ± 0.02ab	2.48 ± 0.06b	2.41 ± 0.03bc	2.37 ± 0.01c
Fresh-dry ratio	B7	2.93 ± 0.03a	2.88 ± 0.05a	2.83 ± 0.01ab	2.72 ± 0.04b	2.68 ± 0.04bc	2.56 ± 0.09c
Stem-leaf ratio	B2	2.48 ± 0.05a	2.48 ± 0.03a	2.51 ± 0.01ab	2.56 ± 0.02b	2.63 ± 0.11c	2.72 ± 0.08d
Stem-leaf ratio	B7	2.21 ± 0.09a	2.20 ± 0.06a	2.24 ± 0.04a	2.32 ± 0.06b	2.41 ± 0.026c	2.54 ± 0.13d
Note: Different lowercase letters stand for significant differences at P < 0.05.

Table 5

Results of two way ANOVA for the effects of varieties (V) and disease (D) on fresh weight, dry weight, fresh-dry ratio and stem-leaf ratio of oat.
Source	df	Fresh weight		Dry weight		Fresh-dry ratio		Stem-leaf ratio
Source	df	F-value	P	F-value	P	F-value	P	F-value	P
V	1	15.829	<0.001	28.222	<0.001	650.508	<0.001	178.510	<0.001
D	5	33.510	<0.001	17.019	<0.001	51.107	<0.001	141.189	<0.001
V×D	5	2.160	0.056	1.722	0.129	0.862	0.59	1.005	0.47

3.4 Effects of LBD (P. agglomerans) on the parameters of feeding value

Crude ash (CA), crude protein (CP), ether extract (EE) and crude fiber (CF) of B2 and B7 were significantly (P < 0.05) affected by LBD. As disease rating increased from 0 to 5, the contents of CA, CP and EE in B2 and B7 decreased, but CF increased (Fig. 2). Comparing with healthy oat, LBD infection separately reduced the average content of CA, CP and EE in B2 and B7 by 13.4%, 23.3% and 27.22%. However, the average content of CF in these oats was increased by about 5.29%. In different oat varieties, the content of CA, CP, EE and CF were also different. B2 had higher CA and CP than B7, while B7 had higher EE and CF than B2 in all disease ratings (Fig. 2). Furthermore, both oat varieties (V) and LBD (D) had significant (P < 0.05) effects on CA, CP, EE and CF of oat, and the interaction of “V×D” was also significant (P < 0.05) (Table 6).

Table 6

Results of two way ANOVA for the effects of varieties (V) and disease (D) on crude ash, crude protein, ether extract and crude fiber of oat.
Source	df	Crude ash		Crude protein		Ether extract		Crude fiber
Source	df	F-value	P	F-value	P	F-value	P	F-value	P
V	1	158.663	<0.001	107.510	<0.001	121.715	<0.001	52.236	<0.001
D	5	255.034	<0.001	36.701	<0.001	55.909	<0.001	270.908	<0.001
V×D	5	27.173	<0.001	5.287	<0.001	6.918	<0.001	10.177	<0.001

The effects of LBD on acid detergent fiber (ADF), neutral detergent fiber (NDF), nitrogen free extract (NFE) and soluble carbohydrate (SC) of B2 and B7 were significant. The contents of ADF, NDF and NFE of B2 and B7 were increased with increasing disease rating from 0 to 5 (Fig. 3A, B and C), conversely, the content of SC in two oat varieties was decreased (Fig. 3D). The average contents of ADF, NDF and NFE in B2 and B7 were increased by 8.89%, 3.53% and 6.27%, respectively, after LBD infection, while the average contents of SC in B2 and B7 was reduced by about 15.79%. Moreover, ADF and NDF of B7 were higher than B2, but the contents of NFE and SC in B2 were higher than B7 under LBD infection and non-infection conditions (Fig. 3). Both oat varieties (V) and LBD (D) had significant (P < 0.05) effects on ADF, NDF, NFE and SC of oat, but the interaction of “V×D” on these parameters was different. “V×D” had significant (P < 0.05) effect on ADF, NDF and SC of oat, but there was no significant effect in “V×D” on NFE (Table 7).

Table 7

Results of two way ANOVA for the effects of varieties (V) and disease (D) on acid detergent fiber, neutral detergent fiber, nitrogen free extract and soluble carbohydrate of oat.
Source	df	Acid detergent fiber		Neutral detergent fiber		Nitrogen free extract		Soluble carbohydrate
Source	df	F-value	P	F-value	P	F-value	P	F-value	P
V	1	10.816	0.002	62.026	<0.001	4.722	0.037	109.393	<0.001
D	5	290.322	<0.001	4.106	0.017	103.636	<0.001	278.884	<0.001
V×D	5	20.399	<0.001	4.411	<0.001	1.386	0.242	2.428	0.034

The calcium and phosphorus of B2 and B7 were significantly (P < 0.05) affected by LBD. Along with the increase of disease ratings, both calcium and phosphorus of B2 and B7 were reduced (Fig. 4). Comparing with healthy oat, the average content of calcium in diseased oat was decreased by 14.21%, while the average content of phosphorus was increased by 20.88%. In all disease ratings, the content of calcium in B7 was higher than it in B2, but the content of phosphorus in B2 was higher than in B7 (Fig. 4). The effects of oat varieties (V) and LBD (D) on calcium and phosphorus in oat were significant (P < 0.05), but their interaction of “V×D” was different. “V×D” had significant (P < 0.05) effect on calcium of oat, but no significant effect was observed in phosphorus (Table 9).

Table 8

Digestible dry matter, dry matter intake and relative feed value of B2 and B7 under 6 disease ratings.
Disease rating	Varieties	Index
Disease rating	Varieties	Digestible dry matter (%DM)	Dry matter intake (%BM)	Relative feed value
0	B2	42.41 ± 1.62c	3.70 ± 0.48c	124.04 ± 1.57c
0	B7	46.63 ± 1.83a	4.17 ± 0.66a	150.77 ± 2.33a
1	B2	42.36 ± 1.26c	3.74 ± 0.49bc	122.78 ± 1.67c
1	B7	46.57 ± 1.37a	4.18 ± 0.57a	150.79 ± 1.31a
2	B2	41.89 ± 1.26c	3.60 ± 0.25cd	116.98 ± 1.21cd
2	B7	45.89 ± 1.12ab	4.07 ± 1.23ab	144.91 ± 2.18ab
3	B2	41.35 ± 1.25cd	3.46 ± 0.62d	110.85 ± 0.86cd
3	B7	44.84 ± 1.19b	3.89 ± 1.03b	135.20 ± 1.24b
4	B2	40.63 ± 1.51d	3.29 ± 0.67e	103.48 ± 0.42d
4	B7	43.56 ± 1.33bc	3.59 ± 0.84cd	121.04 ± 1.43c
5	B2	39.68 ± 1.11d	3.14 ± 0.22e	96.47 ± 0.75d
5	B7	41.95 ± 1.04c	3.23 ± 0.34e	105.16 ± 0.68d
Note: Different lowercase letters stand for significant differences at P < 0.05.

Table 9

Results of two way ANOVA for the effects of varieties (V) and disease (D) on calcium, phosphorus, digestible dry matter, dry matter intake and relative feed value of oat.
Source	df	Calcium		Phosphorus		Digestible dry matter		Dry matter intake		Relative feed value
Source	df	F-value	P	F-value	P	F-value	P	F-value	P	F-value	P
V	1	418.492	<0.001	168.463	<0.001	62.026	<0.001	106.853	<0.001	77.765	<0.001
D	5	542.077	<0.001	479.464	<0.001	536.147	<0.001	3.293	0.017	269.966	<0.001
V×D	5	3.333	0.007	0.547	0.852	4.411	<0.001	15.400	<0.001	12.767	<0.001

DDM, DMI and RFV of two oat varieties were significantly influenced by LBD. As the disease rating increased from 0 to 5, DDM, DMI and RFV of B2 and B7 were significantly (P < 0.05) decreased by LBD, and they all were reduced by 3.67%, 8.91% and 12.03% respectively comparing with healthy oat. Furthermore, different oat varieties had different DDM, DMI and RFV under LBD infected and uninfected conditions. DDM, DMI and RFV of B7 were significantly (P < 0.05) higher than B2 in all disease ratings (Table 8). Both oat varieties (V) and LBD (D) had significant (P < 0.05) effects on DDM, DMI and RFV, and there was a significant “V×D” interaction (P < 0.05) (Table 9).

3.5 Correlations of LBD ( P. agglomerans ) and oat varieties with plant growth, forage yield and feeding value

The structural equation model (SEM) showed that LBD (P. agglomerans) had significantly negative correlations with seedling growth (P < 0.05), forage yield (P < 0.05), nutritional quality (P < 0.05) and feeding value (P < 0.05). Otherwise, seedling growth, forage yield, nutritional quality and feeding value of oat were positively affected by oat varieties. The SEM explained 91%, 77%, 93% and 84% of the variation in seedling growth, forage yield, nutritional quality and feeding value of oat (Fig. 5).

Bacterial leaf blight disease (LBD) caused by P. agglomerans is a new disease on oat first observed in China and other oat growing areas. The early disease symptoms appeared as light to dark yellow spots in leaf tips, and then the yellow leaf spots have spread throughout the inoculated leaves, and diseased leaves withered within 2 weeks. In our experiments we found that LBD infection could not only decrease plant growth, but also result in reductions in forage yield and feeding value of oat. It demonstrates that LBD (P. agglomerans) can directly or in directly cause the loss of forage yield and feeding value of oat. For other crops, LBD caused by Xanthomonas oryzae can also inhibit plant growth of rice, and cause serious yield and quality losses at different rice growth stages (Noh et al., 2007; Palupi et al., 2013). Similarly, the growth, yield and quality of cotton are also reduced by P. agglomerans, which causes boll rot disease of cotton (Liu et al., 2008).

Plant growth parameters (i.e. effective tillers, plant height, leaf length and width, etc.) are the most important agronomic traits in oat and other corps, which are closely related to morphology, green and dry matter production, and even for grain yield and quality (Zsubori et al., 2002). The previous study on P. agglomerans in oat seeds has revealed that it can decrease the seed germination and seedling growth of oat on petri plates (Wang et al., 2022b). In this study with LBD (P. agglomerans), we found that effective tillers, plant height, flag-leaf length and width of B2 and B7 were all decreased by LBD (P. agglomerans) in greenhouse, which demonstrated that plant growth of oat expressed negative correlation with LBD development. Similarly, P. agglomerans caused LBD on rice, which inhibited seed germination, stem and root growth of rice plants (Hong et al., 2002). Furthermore, Díaz-Lago et al. (2002) and Bisnieks et al. (2005) found that diseases caused by Puccinia coronata and BYDV could reduce both plant height and leaf area of oat. These negative influences might be due to the reduction in leaf length and width, which causes decrease in photosynthesis of host plants (Yamori, 2020; Liu et al., 2021).

Plant disease is one of the factors of leading forage or grain yield losses worldwide. The occurrence of these losses is mainly due to disease influence yield components such as effective tillers, plant height, flag-leaf length and width (Chemweno, 2016). Thus, improving or promoting plant growth of oat is important to increase forage and grain yield of oat. Previous studies on P. agglomerans have shown that the grain and stalk yield of maize and rice is reduced by LBD caused by this bacterium (Lee et al., 2010; Juárez et al., 2018). Other diseases induced by P. agglomerans in walnut (Zhu et al., 2014) and onion (Vahling-Armstrong et al., 2015) also caused reduction of yield, and yield loss had close relationship to reduced plant growth. LBD caused by P. agglomerans is a new disease in oat, and it significantly decreased fresh weight, dry weight, fresh-dry ratio and stem-leaf ratio of oat in milking stages. These results demonstrated that LBD (P. agglomerans) could reduce the growth of oat, and growth reduction could also result in forage yield loss. Because of this, it is important to take agricultural, biological, and chemical preventive and control practices that can reduce oat forage yield losses caused by LBD (P. agglomerans).

Oat is very palatable, quick growing with high dry matter production and relatively high nutritive value which is conceived for human consumption and animal feed (Irfan et al., 2016). It is mostly used to make green fodder and hay to produce high quality feed for livestock, because of its high forage yield, nutritional quality and wide adaptability to environment (Tulu et al., 2020). Unfortunately, forage yield and nutritional quality of oat are reduced by diseases, such as crown rust (Puccinia coronata) (Pacheco et al., 2004), powdery mildew (Blumeria graminis) (Montillabascn et al., 2015), loose smut (Ustilago avenae) and leaf blight (Helminthosporium sp.) (Banyal et al., 2016), etc. Similarly, the nutritional qualities of oat, such as crude ash, crude protein, ether extract, soluble carbohydrate, calcium, phosphorus, digestible dry matter, dry matter intake and relative feed value, were decreased by LBD (P. agglomerans), but the content of crude fiber, acid and neutral detergent fiber was increased. It might be due to P. agglomerans reduced the photosynthetic efficiency of oat leaves, which affected the formation and accumulation of nutrients on oat plants based on the previous research results of LBD (P. agglomerans) (Wang et al., 2022c).

There are differences in growth character, forage yield and feeding value between A. nuda and A. sativa, and their resistances to biotic and abiotic stress are also different because of differences in genetic and biological characteristics (Pisulewska et al., 2009; Ma et al., 2010; Sliková et al., 2010; Ta et al., 2010; Hu et al., 2012). Tao et al. (2018) reported that the germination rate, germination index, vigor index, plumule length and radicle length of A. sativa was higher than A. nuda under different NaCl stress conditions, and these results revealed that A. sativa has higher salt resistance than A. nuda. Meanwhile, studies in A. nuda and A. sativa also showed that fresh forage yield, hay yield and crude protein of A. sativa were higher than A. nuda (Wang et al., 2019; Shi, 2019). In this study, the parameters of ET, FLL, FLW, FW, DW, EE, DDM, DMI, RFV and calcium in A. sativa were significantly higher than A. nuda. However, the PH, SLR, CP, CF, ADF and NDF of A. sativa were lower than those of A. nuda. It demonstrated that A. sativa had a higher growth character, forage yield and feeding value than A. nuda under healthy and diseased conditions, but A. nuda expressed relatively greater sensitivity to LBD than A. sativa.

In conclusion, these results demonstrate that LBD induced by P. agglomerans in oat had negative influences on plant growth, forage yield and feeding value, and manifested in reduction in effective tillers (ET), plant height (PH), flag-leaf length (FLL), flag-leaf width (FLW), fresh weight (FW), dry weight (DW), fresh-dry ratio (FDR), crude ash (CA), crude protein (CP), ether extract (EE), soluble carbohydrate (SC), calcium, phosphorus, digestible dry matter (DDM), dry matter intake (DMI) and relative feed value (RFV) of oat. On the contrary, the parameters of crude fiber (CF), acid detergent fiber (ADF) and neutral detergent fiber (NDF) were increased by LBD caused by P. agglomerans. In addition, A. sativa showed higher growth character, forage yield and feeding value than A. nuda after inoculation and non-inoculation with P. agglomerans. These findings suggest that the infection and development of LBD caused by P. agglomerans lead to the reduction in plant growth, forage yield and feeding value of oat, and it is necessary to pursue methods for prevention and control of LBD to reduce crop losses.

Acknowledgments

This study was supported by National Key Research and Development Program of China (No. 2022YFD1300802), National Key R & D Program of China (No. 2022YFD1401101), China Agriculture Research System (CARS-07-C, Oat) and Gansu Provincial Youth Science and Technology Fund Program (22JR5RA532). JFW is thankful for support from USDA-NIFA Multistate Project W4147. The authors would like to thank the anonymous reviewers for their helpful and constructive comments on an earlier version of this manuscript.

Data availability statement

All data used during the study are provided in the paper or are available from the corresponding author upon reasonable request.

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

The research involved neither human participants nor animals in this article.

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Impact of bacterial leaf blight disease ( Pantoea agglomerans ) on forage yield and feeding value of oat

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Abstract

Figures

1. Introduction

2. Materials and methods

2.1 Plant materials

2.2 Bacterial suspension preparation

2.3 Seed treatment and seedling cultivation

2.4 Bacterium inoculation

2.5 Disease rating

2.6 Measurement parameters

2.7 Statistical analysis

3. Results

3.1 ADR and ADI of oat in jointing, flowering and milking stages

3.2 Effects of LBD (P. agglomerans) on the parameters of plant growth

3.3 Effects of LBD (P. agglomerans) on the parameters of forage yield

3.4 Effects of LBD (P. agglomerans) on the parameters of feeding value

4. Discussion

Declarations

References

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