管理制度和土壤气候因素对德国豌豆根相关镰刀菌和双酶菌群落的影响-动脉网

Effect of management system and pedoclimatic factors on Fusarium and Didymella communities associated with pea (Pisum sativum) roots in Germany

Nature 等信源发布 2025-01-21 03:36

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Abstract

摘要

From 2016 to 2019, 128 organic and conventional spring and winter pea fields in Germany were surveyed to determine the effects of cropping history and pedo-climatic conditions on pea root health, the diversity of

Fusarium

镰刀菌

and

和

Didymella

communities and their collective effect on pea yield. Roots generally appeared healthy or showed minor disease symptoms despite the frequent occurrence of 4

群落及其对豌豆产量的集体影响。根通常看起来健康或表现出轻微的疾病症状，尽管经常发生4

Didymella

and 14

和14

Fusarium

镰刀菌

species. Soil pH interacted with the occurrence of the

物种。土壤pH值与

Fusarium oxysporum

Fusarium oxysporum（英语：Fusarium oxysporum）

species complex (FOSC) and

物种复合体（FOSC）和

F. tricinctum

F、三角肌

that correlated with reduced or increased soil pH values, respectively. While legumes in the cropping history or reduced time between legumes correlated with occurrence of

这分别与土壤pH值的降低或增加有关。而种植历史中的豆类或豆类之间的时间缩短与

D. pinodella

D.皮诺德拉

and to a lesser degree with the members of the

在较小程度上与

F. solani

茄病镰刀菌

species complex (FSSC), the reverse was true at least in organic spring peas for

物种复合体（FSSC），至少在有机春豌豆中相反

F. redolens

F. 规律性

. Only in conventional systems increased root infections with

。只有在常规系统中，根部感染才会增加

F. redolens

F. 规律性

and the FSSC were linked to root rot incidence whereas yields negatively correlated with the FOSC and positively with

FSSC与根腐病发病率相关，而产量与FOSC呈负相关，与

F. tricinctum

F、三角肌

isolation frequencies. Overall, this study shows that pea root rot pathobiome is rather stable and that the damage caused is mostly due to the interaction with environmental conditions.

隔离频率。总体而言，这项研究表明，豌豆根腐病病原菌群相当稳定，造成的损害主要是由于与环境条件的相互作用。

Introduction

导言

Peas are an important protein crop as well for human as for animal nutrition well adapted to cool climatic conditions. As leguminous crop, they simultaneously provide important ecological services such as biological N fixation. However, frequently pea production is limited by multiple soil-borne pathogens that cause pre- and postemergence death, wilts and foot and root rots which are collectively referred to as a ‘pea root rot pathogen complex’.

。作为豆科作物，它们同时提供重要的生态服务，如生物固氮。然而，豌豆生产经常受到多种土传病原体的限制，这些病原体会导致出苗前和出苗后死亡，枯萎病以及脚和根腐烂，统称为“豌豆根腐病病原体复合体”。

The diversity and predominance of pathogens in the root rot complex can vary greatly depending on the pedo-climatic conditions, cropping history, geographical location, year and even between years within the same location

根腐病复合体中病原体的多样性和优势可能因土壤气候条件、种植历史、地理位置、年份甚至同一地点的年份而异

. Thus, in Germany, surveys from 2005 to 2007 in conventional spring peas

因此，在德国，2005年至2007年对传统春豌豆的调查

and 2009–2012 in organic spring peas

和2009-2012年有机春豌豆

showed that the primary constituents of the pea root rot pathogen complex were the species

结果表明，豌豆根腐病菌复合体的主要成分是

Didymella pinodella

取消画笔

(syns.

（见。

Phoma medicagins

Phoma 医疗

Phoma pinodella

皮诺德拉Phoma pinodella

Peyronellaea pinodella

佩罗内拉 Pinodella

) typically accompanied by a moderate presence of

)通常伴有中度的

Fusarium redolens

红腐镰刀菌

F. avenaceum

F. 大道

, and the members of the

，以及

F. solani

茄病镰刀菌

(FSSC) and

（FSSC）和

F. oxysporum

F.尖孢菌

(FOSC) species complexes. In contrast, in Canada, the pathogen complex is primarily characterized by the dominance of

（FOSC）物种复合体。相比之下，在加拿大，病原体复合体的主要特征是

Aphanomyces eutheices

真隐孢子菌

and

和

F. avenaceum

F. 大道

, whereas in the USA,

，而在美国，

F. avenaceum

燕麦镰刀菌

and FOSC are the most frequently reported

和FOSC是最常报告的

. Recent studies in France and the UK identified

.最近在法国和英国的研究确定

D. pinodella

D. 皮诺德

and the FOSC, FSSC and

F. redolens

F. 规律性

as the predominant species within the pea root rot complex. Understanding the factors that shape the pea root rot complex pathogen community and their influence on yield is essential for effective disease risk assessment and disease management.

作为豌豆根腐病复合体中的主要物种。了解形成豌豆根腐病复杂病原体群落的因素及其对产量的影响，对于有效的疾病风险评估和疾病管理至关重要。

While peas are the most widely grown grain legume crop in Germany

而豌豆是德国种植最广泛的谷物豆类作物

, pea production in Germany sharply declined by 75% from 163.610 hectares (ha) in 2001 to about 42.000 ha in 2014

，德国的豌豆产量从2001年的163.610公顷急剧下降到2014年的约42000公顷，下降了75%

. Low and instable yields together with high susceptibility to soil-borne pathogens had been discouraging farmers from growing this crop. With the implementation of the Germany protein crop strategy in 2012

.低产和不稳定的产量以及对土传病原体的高度敏感性一直阻碍农民种植这种作物。随着2012年德国蛋白质作物战略的实施

and the EU Common Agricultural Policy (CAP) greening measures in 2015, the trend was reversed and by 2022, pea production was about 107.000 ha. As organic pea production overall has remained relatively stable during the past 20 years

2015年，欧盟共同农业政策（CAP）的绿化措施扭转了这一趋势，到2022年，豌豆产量约为107.000公顷。由于有机豌豆产量在过去20年中总体保持相对稳定

, this increase is primarily due to conventional farmers that are now integrating mostly spring pea into their rotations. Often, these farmers are growing legumes for the first time after more than 10 years, providing a unique opportunity to study the effects of cropping history on pea health. For this, from 2016 to 2019 we conducted yearly surveys on pea root health in conventional and organic peas, to evaluate the impact of farming system (organic versus conventional), pedo-climatic conditions and crop rotation management on root health and root rot pathogens and their influence on pea yield..

，这一增长主要是由于传统农民现在正在将大部分春豌豆纳入轮作。。为此，从2016年到2019年，我们对传统和有机豌豆的豌豆根系健康进行了年度调查，以评估耕作制度（有机与传统），pedo气候条件和作物轮作管理对根系健康和根腐病病原体的影响及其对豌豆产量的影响。。

The specific objectives of the study were to (1) determine the current root health status and examine the identity and prevalence of root rot pathogens associated with spring and winter peas in Germany, (2) determine the effect of cropping systems on root health as well as the diversity of

这项研究的具体目标是（1）确定目前的根系健康状况，并检查与德国春季和冬季豌豆相关的根腐病病原体的身份和流行程度，（2）确定种植制度对根系健康的影响以及

Fusarium

镰刀菌

and

和

Didymella

communities in pea roots and, (3) relate the changes in pea root health, cropping history and pedo-climatic conditions to the variations in the

豌豆根中的群落和（3）将豌豆根健康，种植历史和土壤气候条件的变化与

Fusarium

镰刀菌

and

和

Didymella

communities and pea yield. Additionally, (4) we present findings on the genetic variability of the FOSC and FSSC isolates recovered, and compare results from this study with the outcomes of a parallel survey on faba bean root rot in Germany

社区和豌豆产量。此外，（4）我们介绍了回收的FOSC和FSSC分离株的遗传变异性的发现，并将这项研究的结果与德国蚕豆根腐病平行调查的结果进行了比较

, in order to contribute to a better understanding of root health and pathogen dynamics in these two major protein crops.

。

Results

Environmental and soil conditions of the sampled fields

采样场地的环境和土壤条件

The 133 organic and conventional pea fields sampled represented a wide range of environments with respect to climatic and soil conditions (Tables

在气候和土壤条件方面，采样的133个有机和常规豌豆田代表了广泛的环境（表

and

和

). Sowing conditions ranged from very wet (up to 71 mm of rainfall in the 2 weeks preceding sowing) to completely dry, as well as from very cold (with a minimal mean temperature of −4.9 °C two weeks before sowing) to warm conditions (a maximum mean of 13.8 °C before sowing). Similarly, the conditions during plant emergence varied greatly, with up to 72 mm of rainfall two weeks after sowing to entirely dry periods (Table .

)。播种条件从非常潮湿（播种前2周降雨量高达71毫米）到完全干燥，以及从非常寒冷（播种前两周最低平均温度为-4.9°C）到温暖条件（播种前最大平均温度为13.8°C）。同样，植物出苗期间的条件变化很大，播种后两周至完全干旱期降雨量高达72毫米（表）。

). For spring pea, the driest conditions were recorded in 2018, where a field received as little as 21 mm of rainfall from sowing to sampling. Wettest conditions were observed in 2016, with a spring pea field receiving a 533 mm of rainfall over the same period. In winter peas, the driest conditions were recorded 2016/2017, with a field receiving only 163 mm of rain during the growing season, while the wettest conditions occurred in 2018/2019, where a field received 1001 mm of rainfall from sowing to sampling (Table .

)。对于春豌豆来说，2018年记录了最干燥的条件，从播种到取样，一块田地的降雨量只有21毫米。2016年观察到最潮湿的情况，同期春季豌豆田降雨量为533毫米。在冬豌豆中，2016/2017年记录到最干燥的条件，生长季节田间降雨量仅为163毫米，而2018/2019年发生了最潮湿的条件，从播种到采样，田间降雨量为1001毫米（表）。

Table 1 Variability in pedo-climatic conditions across spring and winter pea fields in organic and conventional farming systems during the 2016–2019 sampling period.

表1 2016-2019年采样期间，有机和常规耕作系统中春季和冬季豌豆田的pedo气候条件变化。

Full size table

全尺寸表

Table 2 Soil clusters formed by grouping fields based on their similarity in soil abiotic properties, along with the number of organic and conventional spring and winter pea fields and roots sampled in each year.

表2根据土壤非生物特性的相似性以及每年采样的有机和常规春季和冬季豌豆田和根的数量，将田地分组形成的土壤簇。

Full size table

全尺寸表

Soil types ranged from light sandy soil (up to 86% sand) to heavy clay soils (up to 50% clay) with pH levels ranging from 5.6 to 7.5 and a high variation in soil organic matter (SOM) content from only 1.1% to up to 5.1% (Table

). The sampled fields grouped into 3 clusters based on their similarities in soil pH, sand, silt, clay and organic matter content. The first two dimensions of the Hierarchical Clustering on Principal Components (HCPC) analysis accounted for 77% of the variance in the dataset, 57% in the first dimension that separated sand dominated fields (Cluster I) from silty-clay soils in Clusters II and III (Table .

)。根据土壤pH值、沙子、淤泥、粘土和有机质含量的相似性，将采样场分为3类。主成分层次聚类（HCPC）分析的前两个维度占数据集中方差的77%，在第一个维度中占57%，第一个维度将砂土为主的田地（第一组）与第二组和第三组中的粉质粘土分开（表）。

). The second dimension explained an additional 20% of the variance and showed the strongest association with SOM content.

)。第二个维度解释了另外20%的方差，并显示出与SOM含量的最强关联。

Cluster I comprised 15 organic and 19 conventional spring pea fields and 2 conventional winter pea fields with sandy soils and a pH of around 6.4. The mean SOM content in Cluster I was 1.8% in organic fields and approximately 2.5% in conventional fields. The largest Cluster II comprised silty-clay soils with mean pH of 6.5 and 2.6% SOM, represented by 39 spring pea fields, 4 of organic and 21 out of the 29 organic winter pea fields.

第一组包括15个有机和19个常规春季豌豆田和2个常规冬季豌豆田，土壤沙质，pH值约为6.4。第一类土壤有机质平均含量在有机田为1.8%，在常规田约为2.5%。最大的第二组由粉质粘土组成，平均pH值为6.5，SOM为2.6%，代表39个春季豌豆田，4个有机豌豆田和29个有机冬季豌豆田中的21个。

Cluster III soils were again silty-clay but with higher pH (about 7.1) and mean SOM contents (3.0 for spring pea and 3.5 for winter pea fields). Four of the 26 spring pea fields and 8 of the 11 winter pea fields were organic (Table .

第三组土壤再次为粉质粘土，但pH值较高（约7.1），平均SOM含量较高（春豌豆为3.0，冬豌豆为3.5）。26个春季豌豆田中的4个和11个冬季豌豆田中的8个是有机的（表）。

Crop rotations

作物轮作

The proportion of legumes in the five years preceding pea sampling varied considerably depending on system and pea type. In 14 out of the 23 organic spring and 27 out of the 29 organic winter pea fields legumes had been cultivated in the five years preceding our sampling (Fig.

豌豆采样前五年的豆类比例因系统和豌豆类型而异。在我们采样前的五年中，23个有机春季中的14个和29个有机冬季豌豆田中的27个种植了豆科植物（图）。

). In contrast, out of the 81 conventional fields sampled, 59 had not been cropped to any legume in that period.

)。相比之下，在抽样的81块常规农田中，有59块在此期间没有种植任何豆类。

Fig. 1

图1

Legumes in organic and conventional crop rotations. (

有机和常规作物轮作中的豆类。（笑声）(

) Spring pea and (

)春豌豆和(

B类

) Winter pea: On the left, the number of fields with legumes grown in the past five years prior to sampling; on the right, the number of fields and the time since legumes were last cultivated before sampling. Data for more than 11 years were not available.

)冬豌豆：左边是采样前过去五年种植豆科植物的田地数量；右边是采样前最后一次种植豆类的田地数量和时间。没有11年以上的数据。

Full size image

全尺寸图像

In half (7) organic spring pea fields with legumes in the past five years, grain legumes had been cultivated once (four times pea and two times faba bean and once, pea and faba bean). Clover and alfalfa were grown on 13 fields either in one out of 5 years (8 fields), or for two (3 fields) or three (2 fields) consecutive years.

在过去五年中，在半（7）个有豆类的有机春豌豆田中，种植了一次谷物豆类（四次豌豆和两次蚕豆，一次豌豆和蚕豆）。三叶草和紫花苜蓿在13块地上生长，每5年一次（8块地），或连续两年（3块地）或三年（2块地）。

All except one organic farms grew cereals, either in one (3 fields), two (2 fields), three (4 fields), four (9 fields) or five (4 fields) years during the preceding 5-years. In addition, eight out of the 23 organic spring pea fields grew this crop in mixture with oats (.

在过去的5年中，除一个有机农场外，所有农场都在一（3场）、两（2场）、三（4场）、四（9场）或五（4场）年份种植谷物。此外，在23块有机春豌豆田中，有8块与燕麦混合种植这种作物。

Avena sativa

燕麦

; 5 fields), false flax (

；5场），假亚麻(

Camelina sativa

亚麻荠

; 2 fields) or spring wheat (

；2块田地）或春小麦(

Triticum aestivum

曲风美学

; 1 field) (Supplementary Table

；1个字段）（补充表

S1级

Grain legumes were present once (9 times), twice (5 times) and trice (once) during the five years before organic winter peas. Out of these 15 cases, 11 fields had been planted with pea, 9 once and 2 twice; faba beans were grown in 4 fields once. Additionally, clover and alfalfa had been grown on 17 fields, either for one (10 fields) or two years (7 fields).

在有机冬豌豆之前的五年中，谷物豆类出现了一次（9次），两次（5次）和三次（一次）。在这15例中，11块地种了豌豆，9块一次，2块两次；蚕豆曾在4块地里种植过一次。。

Cereals had been grown in all 29 fields: 9 times twice and 9 times trice, 10 times for four years, and once in all five years before winter peas. All organic winter peas were grown in mixtures with triticale (19 fields), rye (9 fields) of winter wheat (1 field) (Supplementary Table .

所有29块地都种植了谷物：9次两次和9次三次，4年10次，在冬豌豆之前的五年中有一次。所有有机冬豌豆均与小黑麦（19块地），冬小麦（1块地）的黑麦（9块地）混合种植（补充表）。

S1级

Among the 20 conventional spring pea fields with legumes in the previous five years, 11 had been cultivated with pea once and two twice and one with faba bean. In one of the winter pea fields two years grass-clover and in one faba beans had been grown. Five farmers also had clover and alfalfa based mixtures in the rotations.

在过去五年的20个常规豆类春季豌豆田中，11个用豌豆一次栽培，两次栽培，一个用蚕豆栽培。在一块冬豌豆地里，种植了两年的草三叶草和一块蚕豆。五名农民在轮作中也使用了三叶草和苜蓿的混合物。

The conventional 5-year rotation plans included two (14 fields), three (29 fields), four (23 fields) or five (5 fields) years of cereals. Only two conventional fields had not at all been sown to cereals (Fig. .

传统的五年轮作计划包括两年（14块地）、三年（29块地）、四年（23块地）或五年（5块地）的谷物。只有两块传统的田地根本没有播种谷物（图）。

). Conventional peas were predominantly cultivated as pure stand (73 fields), whereas three spring pea fields were grown in mixture either with barley (2 fields) or false flax (1 field). Among the 5 conventional winter pea fields, two farmers grew the crop in mixture with triticale (Supplementary Table .

)。传统豌豆主要作为纯林（73块地）种植，而三块春豌豆田与大麦（2块地）或假亚麻（1块地）混合种植。在5个传统的冬季豌豆田中，有两个农民将这种作物与小黑麦混合种植（补充表）。

S1级

Field level root rot incidence and root health status

田间根腐病发生率和根系健康状况

Overall, a total of 2560 pea roots were assessed for the severity of root rot symptoms. In spring pea fields (total number of roots assessed,

总体而言，总共评估了2560个豌豆根的根腐症状的严重程度。在春季豌豆田（评估的根总数，

= 1945), root heath status ranged from completely healthy (disease severity rating DSR = 1; absence of any symptoms) to moderately diseased (DSR = 6.1 in organic fields,

1945年），根健康状况范围从完全健康（疾病严重程度评分DSR＝1；无任何症状）至中度患病（有机田DSR=6.1，

= 441 and; DSR = 6.2 in conventional fields,

=441和；DSR在常规领域为6.2，

= 1504). Mean DSR in organic peas (3.0) was significantly higher (

有机豌豆（3.0）的平均DSR明显更高(

= 0.04) than in conventional peas (2.2). Clearly visible symptoms of field level root rot with mean DSR > 3 were recorded in 7 (30%) out of 23 organic and 15 (20%) with no statistically significant year or systems effects (Table

==0.04）比传统豌豆（2.2）高。23种有机物中有7种（30%）和15种（20%）记录了田间水平根腐病的清晰可见症状，平均DSR>3，无统计学意义的年份或系统影响（表

). Root rot was equally severe in the 15 organic spring pea pure stands and the 8 organic species mixtures (Supplementary Table

)。在15个有机春豌豆纯林和8个有机物种混合物中，根腐病同样严重（补充表

S2级

Table 3 Number of fields with field level root rot incidence (disease severity ratings > 3) and mean root rot disease severity ratings (DSR) for organic and conventional pea fields sampled across Germany from 2016 to 2019.

表3 2016年至2019年在德国采样的有机和常规豌豆田的田间根腐病发病率（疾病严重程度评级>3）和平均根腐病严重程度评级（DSR）的田间数量。

Full size table

全尺寸表

Winter peas appeared mostly healthy with overall mean DSR of 2.0 and 1.5 in organic (

冬豌豆看起来大多健康，有机物的总体平均DSR分别为2.0和1.5(

= 29;

= 29；

= 515) and conventional (

515）和常规(

= 5;

=5；

= 100) fields, respectively. Moderate field level root rot was recorded only on two organic winter pea fields (7%) sampled in 2017 with mean DSR of 4.3 and 5.5 (Table

。仅在2017年采样的两个有机冬豌豆田（7%）上记录到中度田间根腐病，平均DSR为4.3和5.5（表

Fusarium

镰刀菌

and

和

Didymella

species associated with pea roots

与豌豆根有关的物种

A total of 5097 isolates representing 4

共有5097个分离株，代表4个

Didymella

and 14

和14

Fusarium

镰刀菌

spp. were recovered from 2651 roots used for the fungal isolations over the 4-yr study period (Supplementary Table

在4年的研究期间，从2651根用于真菌分离的根中回收了属（补充表）

S1级

). With 56% of all roots infected,

)。56%的根被感染，

D. pinodella

D. 皮诺德

was the most frequently recovered species, followed by

是最常被回收的物种，其次是

F. redolens

F. 规律性

F. avenaceum

F. 大道

and the members of the FOSC with approximately 27% infected roots. Members of the FSSC (18% roots infected) and the species

以及FOSC成员中约27%的感染根。

F. tricinctum

F、三角肌

(14%) were the next most frequently isolated.

（14%）是第二个最常被隔离的。

Fusarium equiseti

马镰孢菌

and

和

F. culmorum

黄色镰刀菌

were found with overall root infection rates of about 5%. Also found but represented with few isolates only were the species

发现总体根部感染率约为5%。也发现但仅以少数分离株为代表的是该物种

F. acuminatum

F、尖锐湿疣

F. graminearum

F.禾谷镰刀菌

F. sporotrichioides

F.孢子虫

F. crookwellense

F、克罗克韦伦

F. torulosum

F. 管道

F. flocciferum

F.絮状物

F. sambucinum

F.桑布菊粉

D. pinodes

D、皮诺德斯

D. lethalis and D. eupyrena (

D、致死率和D.eupyrena(

syn.

同步。

Juxtiphoma eupyrena).

eupyrena斑疹伤寒）。

Isolation frequencies varied significantly depending on the fungal species (

分离频率因真菌种类而异(

< 0.0001), pea type (spring vs. winter,

，豌豆类型（春季与冬季，

= 0.002) and year (

=0.002）和年份(

= 0.005) with significant interactions between fungal species isolation frequencies and pea type, growing system and year (

= 0.005），真菌物种分离频率与豌豆类型、生长系统和年份之间存在显著的相互作用(

< 0.0001). Organic spring pea roots were infected more frequently with

<0.0001）。有机春豌豆根感染率更高

D. pinodella

D.皮诺德拉

(

= 0.005) and members of the FOSC (

= 0.005）和FOSC成员(

= 0.003) compared to conventional spring peas (Fig.

=0.003）与传统的春豌豆相比（图）。

). The higher overall isolation frequencies of

)。整体隔离频率较高

D. pinodella

D. 皮诺德

in organic systems compared to conventional were mainly due to higher frequencies of this species in 2016 and 2017 in organic fields compared to the conventional (ca. 70% infected roots in organic systems vs. ca. 40% infected roots in conventional systems). In 2018 and 2019, the species showed similar frequencies in both management systems (ca.

与常规相比，在有机系统中，主要是由于2016年和2017年该物种在有机领域的频率高于常规（有机系统中约70%的感染根与常规系统中约40%的感染根）。在2018年和2019年，该物种在两个管理系统中显示出相似的频率（约。

30 and 60% roots infected in 2018 and 2019, respectively). The FOSC members were consistently 10–20% more frequent in roots collected from organic (35–51%) compared to conventional systems (28–35%), but these differences were not statistically significant (Supplementary Table .

2018年和2019年分别有30%和60%的根被感染）。与传统系统（28-35%）相比，从有机物（35-51%）收集的根中，FOSC成员的频率始终高出10-20%，但这些差异在统计学上并不显着（补充表）。

S3级

). In contrast to FOSC and

)。与FOSC和

D. pinodella

D.皮诺德拉

, organic spring pea roots were less frequently infected with

，有机春豌豆根感染频率较低

F. tricinctum

F、三角肌

(

= 0.0006) and

=0.0006）和

F. culmorum

黄色镰刀菌

(

= 0.006) compared to conventional although at overall low frequencies. Isolation frequencies of

==0.006）与传统频率相比，尽管总体频率较低。隔离频率

F. redolens

F. 规律性

(

= 0.08), the FSSC (

= 0.08），FSSC（

= 0.6),

= 0.6，

F. avenaceum

F. 大道

(

= 0.01) and

=0.01）和

F. equiseti

F. 马匹

(

= 0.01) varied somewhat among years with no statistically significant effect of management system (Fig.

= 0.01）在不同年份之间有所不同，管理系统的影响无统计学意义（图）。

and Supplementary Table

和补充表

S3级

). None of the isolation frequencies of the individual fungal species was affected by species mixtures in organic spring peas (Supplementary Table

)。有机春豌豆中的物种混合物不影响单个真菌物种的分离频率（补充表）

S2级

Fig. 2

图2

Effect of management system on isolation frequency (%) of the top eight fungal species recovered from spring and winter pea roots. Asterisks indicate significant differences (

管理制度对春季和冬季豌豆根中前八种真菌分离频率（%）的影响。星号表示显着差异(

< 0.05) between organic and conventional fields for each fungal species separately (Sidak-adjusted pairwise least significant means comparisons). The horizontal line in the boxplot shows the median value, the bottom and tops of the box the 25th and 75th percentiles and the vertical lines the minimum and maximum values, outliers as single points.

（Sidak调整的成对最小显着性均值比较）。箱线图中的水平线显示中值，框的底部和顶部为第25和第75百分位数，垂直线为最小值和最大值，异常值为单点。

Mean values are marked with triangles..

平均值用三角形标记。。

Full size image

全尺寸图像

On average, 89% (72–98%) of the organic winter pea roots were infected with

平均而言，89%（72-98%）的有机冬豌豆根被感染

D. pinodella

D.皮诺德拉

. Infections with

.感染

Fusarium

镰刀菌

spp. were considerably lower (Fig.

spp.相当低（图）。

and Supplementary Table

和补充表

S3级

) with

)与

F. avenaceum

F. 大道

most frequently recovered (27% overall mean isolation frequencies), followed by

恢复频率最高（总体平均隔离频率为27%），其次是

F. redolens

F. 规律性

and the FSSC (9%). The remaining

和FSSC（9%）。剩下的

Fusarium

镰刀菌

species occurred overall at frequencies of 6% and lower (Fig.

物种总体发生频率为6%或更低（图）。

and Supplementary Table

和补充表

S3级

). Conventional winter pea roots followed a similar trend with

)。传统的冬豌豆根也有类似的趋势

D. pinodella

D.皮诺德拉

(58%) predominant, followed by

F. avenaceum

F. 大道

(22%) and

（22%）和

F. redolens

F. 规律性

(19%) (these data were not included in any statistical analysis due to very small sample size (

（19%）（由于样本量很小，这些数据未包括在任何统计分析中(

= 5)) (Fig.

= 5）（图。

and Supplementary Table

和补充表

S3级

Phylogeny

系统发育

Based on the single-locus phylogeny the 30 FSSC isolates belonged to three different lineages, all nested within clade 3 (Fig.

基于单基因座系统发育，30个FSSC分离株属于三个不同的谱系，全部嵌套在进化枝3内（图）。

). The majority of the isolates (28 out of 30) closely matched

)。大多数分离株（30个中的28个）紧密匹配

Fusarium vanettenii (

Fusarium vanettenii （

syn.

同步。

F. pisi

F. 尿

F. solani

茄病镰刀菌

f. sp.

f、。

pisi

小便

). In addition, one isolate was placed within the

)。此外，一个分离株被放置在

F. solani

茄病镰刀菌

sensu stricto lineage, and one isolate matched

严格意义上的血统，一个分离株匹配

F. breviconum

F.短锥虫

Fig. 3

图3

The maximum likelihood (RAxML) tree constructed using partial

使用部分构造的最大似然（RAxML）树

tef1

alpha gene sequences from 30 isolates of the

来自30个分离株的α基因序列

Fusarium solani

茄病镰刀菌

species complex (FSSC) examined in this study highlighted in bold and red (i.e. FOEP-this study). FOSC isolates from parallel previous study

本研究中检查的物种复合体（FSSC）以粗体和红色突出显示（即本研究中的FOEP）。FOSC分离自先前的平行研究

recovered from faba bean were also included in the analysis were also included in the analysis (FOEP isolates). Epi- and ex-type strains are marked with a ‘T’

从蚕豆中回收的也包括在分析中，也包括在分析中（FOEP分离株）。Epi型和ex型菌株标有“T”

. The scale bar represents 0.04 expected changes per site, and the tree is rooted with

。比例尺表示每个站点的预期变化为0.04，树的根为

F. thapsinum

F.thapsinum

(H05557S1 DCPA).

（H05557S1 DCPA）。

Full size image

全尺寸图像

The 17 FOSC isolates were nested within six clades (Fig.

17个FOSC分离株嵌套在六个进化枝中（图）。

). The largest group consisting of 6 isolates (clade 8 in this study) showed the closest genetic relationship to the previously classified

)。由6个分离株组成的最大群体（本研究中的进化枝8）显示出与先前分类的最接近的遗传关系

F. oxysporum

F.尖孢菌

forma specialis (f. sp.)

特殊形式（e. sp.）

pisi

小便

(PG108; MIAE 08036) and f. sp.

（第108页；MIAE 08036）和f.sp。

conglutinans

合并

(NRRL 36364). Two isolates were associated with clade 7, described as the

（NRRL 36364）。两个分离株与进化枝7相关，被描述为

F. fabacearum

F. 植物

and

和

F. gossypinum

F.棉蚜

in Lombard et al. (2019) which were not entirely resolved in our single-locus analysis. In addition, individual isolates were nested within clades 5 and 13 corresponding to the previously described

在Lombard等人（2019）中，我们的单基因座分析并未完全解决。此外，单个分离株嵌套在进化枝5和13中，对应于前面描述的

F. cugenangense

F.致癌性

and

和

F. odoratissimum

F. 最有气味

(Lombard et al., 2019).

（Lombard等人，2019）。

Fig. 4

图4

The maximum likelihood (RAxML) tree constructed based on partial

基于部分的最大似然（RAxML）树构造

tef1

alpha gene sequences from isolates of the

Fusarium oxysporum

Fusarium oxysporum（英语：Fusarium oxysporum）

species complex (FOSC) used in this study, highlighted in bold and red (e.g., FOEP-this study). The FOSC isolates from parallel previous study

本研究中使用的物种复合体（FOSC），以粗体和红色突出显示（例如，本研究中的FOEP）。FOSC从先前的平行研究中分离出来

recovered from faba bean were also included in the analysis and are indicated in red with host in brackets. Along with the FOSC clades are given proposed species names in the FOSC along with epi- and ex-type strains (in bold) suggested by Lombard et al.

从蚕豆中回收的也包括在分析中，用红色表示，括号中有宿主。与FOSC进化枝一起，在FOSC中给出了拟议的物种名称，以及Lombard等人提出的epi和ex型菌株（粗体）。

. The scale bar represents 0.005 expected changes per site, and the tree is rooted with

。比例尺表示每个站点0.005个预期变化，树的根为

F. udum

F.udum

(CBS 177.31).

（哥伦比亚广播公司第177.31页）。

Full size image

全尺寸图像

The relationship between pathogen occurrence, root health, yield and environmental factors

Cool temperatures in early spring favored

早春适宜凉爽的气温

F. redolens

F. 规律性

in organic winter peas and both, organic and conventional spring peas were favored by cool temperatures in early spring. In addition, in spring peas, the species was overall reduced in wetter years, and only in organic systems if more grain legumes occurred in the rotation (Table

在有机冬豌豆和两者中，有机和常规春豌豆在早春受到凉爽温度的青睐。此外，在春豌豆中，该物种在湿润年份总体减少，只有在轮作中出现更多谷物豆类的情况下，该物种才会在有机系统中减少（表

Table 4 Summary of Pearson correlation analysis results, demonstrating key environmental and cropping history factors impacting pea yield and the abundance (isolation frequencies) of major fungal species in the roots of organically (org.) and conventionally (conv.) cultivated spring and winter pea. Positive correlations are indicated with ‘+’ and indicate increase in the species isolation frequencies (root colonization rates).

表4 Pearson相关分析结果总结，证明了影响豌豆产量的关键环境和种植历史因素以及有机（有机）和常规（转化）栽培春豌豆和冬豌豆根中主要真菌物种的丰度（分离频率）。正相关用“+”表示，表明物种分离频率（根定植率）增加。

Negative correlations are indicated with ‘-’ and indicate decrease in the species isolation frequencies (root colonization rates). .

负相关用“-”表示，表明物种隔离频率（根定植率）降低。

+/- early cold: positive (+) or negative (-) correlation with Average temp. °C (Jan-sowing) and/or, Number of days < 5°C (14 days prior to or after sowing-sowing) and/or, Number of days < 0° in March and/or, Average temp. °C (14 days prior to sowing-sowing) and/or, Number of days < 5°C (sowing-14 days after).

+/-早寒：与平均气温（°C）（1月播种）和/或，日数<5°C（播种前或播种后14天）和/或，3月日数<0°和/或平均气温（°C）（播种前14天）和/或日数<5°C（播种后14天）呈正（+）或负（-）相关。

+ warm season: positive correlation with Average temp. or temp. sum °C (sowing-root sampling); +cool season: negative correlation with Average temp. or temp. sum °C (sowing-root sampling).

++冷季：与平均气温或总气温呈负相关（播种根取样）。

+/- early wet: positive (+) or negative (-) correlation with Precipitation sum (mm) (28 days before sowing to sowing) and/or, Precipitation sum (mm) (sowing to14 days after).

+/-早期湿润：与降水总量（mm）（播种前28天至播种后）和/或降水总量（mm）（播种后14天）呈正（+）或负（-）相关。

+dry season: negative correlation with Precipitation sum (mm) (sowing-root sampling).

+旱季：与降水总量（mm）呈负相关（播种根取样）。

Full size table

全尺寸表

The members of the FOSC in organic and conventional spring peas were negatively correlated with pH and in conventional systems with cluster III soils while cluster I soils favored their occurrence. In contrast, in organic winter peas overall warm temperatures and wet conditions correlated with FOSC occurrence.

有机和常规春豌豆中的FOSC成员与pH呈负相关，在常规系统中与III类土壤呈负相关，而I类土壤有利于它们的发生。相反，在有机冬豌豆中，整体温暖的温度和潮湿的条件与FOSC的发生相关。

The isolation frequencies of the FSSC members correlated positively only with the frequency of grain legumes in the rotation under conventional conditions. No significant effects of environmental conditions in organic systems could be found (Table .

在常规条件下，FSSC成员的隔离频率仅与轮作中谷物豆类的频率呈正相关。在有机系统中没有发现环境条件的显着影响（表）。

Warmer temperatures during the season affected

受影响季节气温升高

F. avenaceum

F. 大道

in organic spring peas negatively while in conventional spring peas, it was favored by higher humidity. In organic winter peas this species correlated negatively with the clay content of the soil (Table

在有机春豌豆中呈负相关，而在常规春豌豆中，较高的湿度有利于其生长。在有机冬豌豆中，该物种与土壤的粘土含量呈负相关（表

In conventional spring peas,

在传统的春豌豆中，

F. tricinctum

F、三角肌

was positively correlated with warm temperatures before sowing, cereals in the rotation and the soil pH and sand contents. The positive association with pH was also observed in winter peas. In organic spring peas, it only correlated with wetter conditions during the season. In spring peas

与播种前的温暖温度，轮作中的谷物以及土壤pH和含沙量呈正相关。在冬豌豆中也观察到与pH的正相关。在有机春豌豆中，它仅与该季节的湿润条件相关。春天的豌豆

F. equiseti

F. 马匹

was not affected by environmental conditions while in organic winter peas the species correlated positively with warmer temperatures during the season (Table

不受环境条件的影响，而在有机冬豌豆中，该物种与该季节的气温升高呈正相关（表

The main factor correlating with increased

与增加相关的主要因素

D. pinodella

D.皮诺德拉

in all growing systems was the cropping history. Both, in conventional spring peas and organic winter peas, the longer the break since the last grain legumes were grown the lower the frequency of

在所有种植系统中都有种植历史。在传统的春豌豆和有机冬豌豆中，自最后一种谷物豆类种植以来，休息时间越长，频率越低

D. pinodella

D.皮诺德拉

isolations. In organic spring peas, instead, the species correlated with the years since conversion to organic which in fact also is an indicator of legume frequency in the system. In organic spring peas, an overall warm season enhanced the frequency while good water supply after sowing was associated with reduced infections.

隔离。相反，在有机春豌豆中，物种与转化为有机后的年份相关，这实际上也是系统中豆科植物频率的指标。在有机春豌豆中，整体温暖的季节提高了频率，而播种后良好的供水与减少感染有关。

In contrast, in winter peas warm conditions with good water supply around sowing reduced .

相反，在冬季，豌豆温暖的条件下，播种周围的良好供水减少。

D. pinodella

D. 皮诺德

root infection rates (Table

根部感染率（表

Except for

除了

F. redolens

F. 规律性

and the FSSC complex in the conventional spring peas none of the fungal species identified correlated with field level root rot incidence, i.e. disease severity > 3 (Table

常规春豌豆中的FSSC复合物没有一种真菌种类与田间根腐病发生率相关，即疾病严重程度>3（表

Water availability, cropping history and soil properties correlated with organic spring pea yields in various ways but not for conventional spring peas or organic winter peas (Table

). Only conventional yields appeared to be weakly affected by the frequencies of root associated

)。只有常规产量似乎受到根系相关频率的微弱影响

Fusarium

镰刀菌

and

和

Didymella

spp. but in part with contradictory trends. Correlations were negative with the FOSC (

但部分趋势相互矛盾。与FOSC呈负相关(

= −0.34) complex but positive with

=-0.34）复杂但积极

F. tricinctum

F、三角肌

(

= 0.34) (Table

=====0.34）（表

Discussion

讨论

Pea roots appeared mostly healthy irrespective of the highly variable pedo-climatic conditions and rotational histories of the 128 organic and conventional spring and winter pea fields sampled. Despite this, 14

无论采样的128个有机和常规春季和冬季豌豆田的高度变化的土壤气候条件和旋转历史如何，豌豆根似乎大多健康。尽管如此，14

Fusarium

镰刀菌

spp. and 4

spp.和4

Didymella

spp. were isolated, including

分离出种属，包括

D. lethalis

D、致命性

and

和

F. flocciferum

F.絮状物

which were identified for the first time in Germany

在德国首次发现

Didymella pinodella

Didyme 的

was the predominant species, followed by

是主要物种，其次是

F. redolens

F.重新设计

F. avenaceum

燕麦镰刀菌

and members of the

以及

Fusarium oxysporum

Fusarium oxysporum（英语：Fusarium oxysporum）

species complex (FOSC). These findings agree with previous reports from Germany which also found similar spectra of these potentially pathogenic fungi in symptomatic pea roots

物种复合体（FOSC）。这些发现与德国先前的报道一致，德国先前的报道也在有症状的豌豆根中发现了这些潜在致病真菌的相似光谱

and predominantly asymptomatic faba bean

主要是无症状蚕豆

roots. Winter pea roots in particular appeared healthy. These cultivars typically have a higher tannin content than spring peas

根。尤其是冬豌豆的根看起来很健康。这些品种的单宁含量通常高于春豌豆

. This may have contributed to the higher resistance and absence of symptom expression which makes them particularly attractive to organic farmers. In contrast, most winter pea varieties are not attractive to conventional farmers due to their indeterminate growth which requires a support crop and poses technical challenges in planting and harvesting including the low economic value of the crop.

。这可能导致更高的抗性和没有症状表现，这使得它们对有机农民特别有吸引力。相比之下，大多数冬豌豆品种对传统农民没有吸引力，因为它们的生长不确定，需要支持作物，并且在种植和收获方面提出了技术挑战，包括作物的低经济价值。

Consequently, all winter pea farmers included in this study cultivated this crop in mixtures and they were predominantly organic..

因此，本研究中包括的所有冬豌豆农民都混合种植这种作物，并且主要是有机作物。。

Phylogenetic analysis inferred from the

从系统发育分析推断

tef1

gene sequences placed the 17 FOSC isolates in 6 clades, all previously associated with pea and/or faba bean roots. This high phylogenetic diversity observed has been reported in other studies

基因序列将17个FOSC分离株置于6个进化枝中，所有这些以前都与豌豆和/或蚕豆根相关。其他研究也报道了这种高度的系统发育多样性

and likely is a result of the polyphyletic origin of different

可能是由于不同的多系起源

F. oxysporum

F. 氧球菌

formae speciales

特殊形式

. Additional analyses are needed to determine the role of these isolates in the pea root rot complex. This is particularly important as the FOSC members also includes endophytes with non-pathogenic characteristics. Also, the characteristics of the different FOSC isolates found in the same host plant but belong to different genetic lineages are not well understood.

。需要进一步的分析来确定这些分离株在豌豆根腐病复合体中的作用。这一点特别重要，因为FOSC成员还包括具有非致病性特征的内生菌。此外，在同一寄主植物中发现的不同FOSC分离株的特征但属于不同的遗传谱系尚不清楚。

These isolates/lineages may potentially show high variation in aggressiveness or specific cultivar-pathogen interactions..

这些分离株/谱系可能在侵袭性或特定品种-病原体相互作用方面表现出高度差异。。

In contrast, the FSSC isolates were phylogenetically less diverse than FOSC, with most belonging to the

相比之下，FSSC分离株的系统发育多样性低于FOSC，其中大多数属于

Fusarium vanettenii

Fusarium Vanettenii

lineage (syn.

血统（syn。

F. pisi

F. 尿

F. solani

茄病镰刀菌

f. sp.

f、。

pisi

小便

). One isolate was placed within the

)。一个分离物被放置在

F. solani

茄病镰刀菌

sensu stricto lineage, and one isolate matched

严格意义上的血统，一个分离株匹配

F. breviconum

F.短锥虫

. These results are consistent with previous studies which also reported similar phylogenetic diversity including the broader host range for the single FSSC isolates recovered from roots of several legumes including pea, faba bean, subterranean clover, white clover and winter vetch

这些结果与先前的研究一致，先前的研究也报道了类似的系统发育多样性，包括从几种豆类（包括豌豆，蚕豆，地下三叶草，白三叶草和冬季紫云英）的根中回收的单个FSSC分离株的更广宿主范围

Higher levels of root rot symptoms in conventional spring pea fields correlated with higher isolation frequencies of

F. redolens

F. 规律性

and the FSSC. In contrast, in organic systems field level root rot incidence was recorded in approximately 30% of the fields but could not be linked to any of the major fungal species isolated. Under organic conditions, the lack of correlation between root health parameters (i.e. visible damage) and fungal species specific isolation frequencies as well as between these parameters and yield, could be due to the stronger impacts of soil conditions as inputs are severely limited.

和FSSC。相比之下，在有机系统中，大约30%的田地记录了田间水平的根腐病发病率，但不能与任何分离的主要真菌物种相关联。在有机条件下，根系健康参数（即可见损伤）与真菌物种特异性分离频率之间以及这些参数与产量之间缺乏相关性，可能是由于土壤条件的影响较大，因为输入受到严重限制。

In addition, factors not evaluated in this study such as weed infestation, insect populations and other physicochemical soil conditions can overshadow the direct influence of root-health related factors on yields and infection rates of potentially pathogenic and other root-associated fungi..

此外，本研究中未评估的因素，如杂草侵染，昆虫种群和其他理化土壤条件，可能掩盖了根系健康相关因素对潜在致病性和其他根系相关真菌的产量和感染率的直接影响。。

While management system (organic vs. conventional) or pea type (spring vs. winter) did not affect the spectrum of fungal species isolated, differences in isolation frequencies were present especially for

虽然管理系统（有机与传统）或豌豆类型（春季与冬季）不影响分离的真菌种类的光谱，但分离频率的差异尤其存在于

D. pinodella.

D、堆叠。

This can be explained mostly by the overall lower frequency of legumes in the conventional cropping histories as repeated grain legume cropping has been shown to result in increased

这主要可以用传统种植历史中豆类的总体频率较低来解释，因为重复种植谷物豆类已被证明会导致增加

D. pinodella

D.皮诺德拉

abundance in soil and roots of pea and faba bean

豌豆和蚕豆的土壤和根系丰度

. The predominance of

.优势

D. pinodella

D. 皮诺德

over

结束

Fusarium

镰刀菌

spp. in organic winter pea roots also agrees with previous results

有机冬豌豆根中的spp.也与先前的结果一致

. The high root infection rates by

.高根感染率

D. pinodella

D. 皮诺德

in organic winter peas compared to organic spring peas further suggest an ecological advantage of this species in cooler and moist environments compared to

与有机春豌豆相比，有机冬豌豆进一步表明，与有机春豌豆相比，该物种在凉爽潮湿的环境中具有生态优势

Fusarium

镰刀菌

spp. Infection success of

spp.感染成功

D. pinodella

D. 皮诺德

is especially high directly after sowing and quickly declines within a few days especially in the presence of beneficial microorganisms such as

播种后直接含量特别高，并且在几天内迅速下降，特别是在存在有益微生物的情况下，例如

F. equiseti

F. 马匹

. It is also possible that the generally higher tannin content in winter peas along with variations in root exudation played a role in modulating the plant-associated microbiome and suppressing

。冬豌豆中通常较高的单宁含量以及根系分泌物的变化也可能在调节植物相关微生物组和抑制中起作用

Fusarium

镰刀菌

infections.

感染。

In both, organic and conventional systems FOSC isolation frequencies negatively correlated with soil pH a fact that has been repeatedly reported

在有机系统和常规系统中，FOSC隔离频率与土壤pH值呈负相关，这一事实已被反复报道

. As organic fields were primarily characterized by sand dominated low SOM soils (Cluster I) and lower pH levels while in conventional systems, silty soils (Cluster II) predominated (Table

由于有机田的主要特征是以沙为主的低SOM土壤（第一组）和较低的pH值，而在常规系统中，以粉土（第二组）为主（表

), it is likely that the abundance of FOSC in organically grown spring peas is at least partly due to the soil characteristics. Lower SOM and soil pH levels typically are characteristic of sandy soils. Such soils mostly have reduced water retention capacity resulting in lower yields of both peas (as observed in this study) and faba beans.

)，有机种植的春豌豆中FOSC的丰度可能至少部分归因于土壤特性。较低的SOM和土壤pH值通常是砂土的特征。这些土壤大多具有降低的保水能力，导致豌豆（如本研究中观察到的）和蚕豆的产量降低。

as yield of both crops highly depend on soil water availability. With yields already impeded in the sandy low SOM fields, the impact of FOSC on yield may not have been distinguishable any more in contrast to its impacts in the better conventional soils.

由于两种作物的产量在很大程度上取决于土壤水分的有效性。由于沙质低有机质农田的产量已经受到阻碍，与在更好的常规土壤中的影响相比，FOSC对产量的影响可能不再明显。

The cereal dominated conventional field histories resulted in higher isolation frequencies of

谷物为主的常规田间历史导致较高的隔离频率

F. tricintum

F.三联针

and likely contributed to increased frequencies of

并可能导致

F. culmorum

黄色镰刀菌

in conventional spring pea roots compared to organic.

与传统的春季豌豆根相比，有机。

Fusarium tricintum

Fusarium 三

also correlated positively with soil pH and negatively with sand. The two species are typical members of the

也与土壤pH值呈正相关，与沙子呈负相关。这两个物种是

Fusarium

镰刀菌

complex associated with ear, stem and root rots in various small-grain cereals and maize and are responsible for pre-harvest mycotoxin contamination

与各种小谷物和玉米中的穗、茎和根腐烂有关的复合物，是造成收获前真菌毒素污染的原因

. However, these species are usually of minor importance in the pea root rot complex and their roles are not fully understood. Thus, conventional spring pea yields actually correlated positively with the abundance of

然而，这些物种在豌豆根腐病复合体中通常不太重要，它们的作用尚不完全清楚。因此，传统的春豌豆产量实际上与

F. tricintum

F. tricintum（英语：F. tricintum）

in roots, a relationship we also found in faba beans

在根中，我们在蚕豆中也发现了这种关系

. In contrast,

相比之下，

F. tricinctum

F、三角肌

has been to be reported potentially important pathogen of soybeans

据报道，大豆的潜在重要病原体

Fusarium culmorum

镰刀菌半岛

is often implicated as a weakly to moderately aggressive pea root rot pathogen

通常被认为是一种弱至中度侵袭性的豌豆根腐病病原体

The wide spread occurrence of

广泛发生的

F. redolens

F. 规律性

F. avenaceum

燕麦镰刀菌

F. equiseti

木贼镰刀菌

and the members of the FSSC in spring peas in both management systems over a range of soil and environmental conditions indicates their good adaptation to diverse pedo-climatic conditions. With the exception of

在一系列土壤和环境条件下，管理系统中春豌豆的FSSC成员表明它们对不同的土壤气候条件有很好的适应能力。除了

F. equiseti

F. 马匹

which has been shown to contribute to disease reduction in various crops

这已被证明有助于减少各种作物的疾病

including pea root rot

包括豌豆根腐病

, all of the remaining

，其余所有

Fusarium

镰刀菌

species are a major part of the pea root rot complex across different climatic and soil conditions, including Canada, France, USA and Germany.

该物种是不同气候和土壤条件下豌豆根腐病复合体的主要组成部分，包括加拿大，法国，美国和德国。

Consistent with recent results in spring faba bean

与春季蚕豆的最新结果一致

, abundance of

，丰富的

F. redolens

F.重新设计

in spring pea roots correlated with cold conditions early in the season during sowing and plant emergence followed by a dry growing season. This highlights the importance of abiotic plant stressors in enhancing the colonization process by this potential pathogen, likely contributing to the higher abundance of this species in conventional pea roots with clear symptoms of root rot.

在春季，豌豆根在播种和植物出苗期间与季节早期的寒冷条件相关，然后是干燥的生长季节。这突出了非生物植物应激物在增强这种潜在病原体的定殖过程中的重要性，可能有助于在具有明显根腐症状的常规豌豆根中增加该物种的丰度。

Interestingly, in organic spring peas .

有趣的是，在有机春豌豆中。

F. redolens

F. 规律性

correlated negatively with frequency of grain legumes in the rotation. This is in contrast to recent reports from Canada

与轮作中谷物豆类的频率呈负相关。

and Germany

和德国

where increased abundance of this fungus positively correlated with grain legume-intensive rotations. These differences could be due to a combination of factors specific to this study, including the influence of prior legume crops and/or other soil and agronomic practices. These factors may have shaped the pea root rot complex community potentially favoring accumulation of more specialized fungal species like .

这种真菌的丰度增加与谷物-豆类密集轮作呈正相关。这些差异可能是由于本研究特有的因素的组合，包括先前豆类作物和/或其他土壤和农艺措施的影响。。

D. pinodella

D. 皮诺德

at the expense of

F. redolens

F. 规律性

. It is also possible that specific soil suppressiveness against

。也可能是特定的土壤抑制作用

F. redolens

F. 规律性

that depends on the regular cropping of grain legume species played a role. A more in-depth microbial community analysis could help elucidate the interaction of cropping system and the broader microbial community structure in influencing the symptom expression and the presence or suppression of single pea pathogens.

这取决于豆科作物的常规种植种类所起的作用。。

We also cannot exclude the possibility of the isolation procedure contributing to these results. The choice of agar medium and the inherent challenges of culture-based methods to recover specific fungal species have been reported previously.

我们也不能排除隔离程序有助于这些结果的可能性。先前已经报道了琼脂培养基的选择以及基于培养的方法恢复特定真菌物种的固有挑战。

. To overcome these limitations DNA-based detection techniques like quantitative real-time (q)PCR assays or next generation sequencing (NGS) could be employed. However, qPCR assays targeting all major fungal species identified in this study have become available only after the start of this research.

为了克服这些局限性，可以使用基于DNA的检测技术，例如定量实时（q）PCR分析或下一代测序（NGS）。然而，针对本研究中鉴定的所有主要真菌物种的qPCR测定仅在本研究开始后才可用。

. Additionally, the application of NGS was beyond the scope and focus of this study, which was primarily focused on examining the occurrence of

此外，NGS的应用超出了本研究的范围和重点，本研究主要集中在检查

Fusarium

镰刀菌

and

和

Didymella

species, their genetic diversity and interactions with cropping systems and yield.

物种，它们的遗传多样性以及与种植制度和产量的相互作用。

The positive correlations of

的正相关

F. avenaceum

燕麦镰刀菌

with cold seasons in organic spring peas and, wet seasons in conventional spring peas, suggest that abiotic plant stress enhances the colonization process by

有机春豌豆的寒冷季节和常规春豌豆的潮湿季节表明，非生物植物胁迫通过

F. avenaceum

燕麦镰刀菌

. While this species plays a significant role in the pea root rot complex in Canada and the USA

虽然该物种在加拿大和美国的豌豆根腐病复合体中起着重要作用

it is mostly an opportunistic pathogen in Germany where it has also been shown to be favored by cool and water logged conditions over winter

在德国，它主要是一种机会性病原体，冬季凉爽和积水的条件也证明了它的优势

In organic systems, the FSSC frequencies were not affected by any of the pedo-climatic or rotational history characteristics tested while under conventional conditions it correlated with root rot incidence and a higher frequency of grain legumes in the rotation. This fungal complex is known to be of importance in pea root health.

在有机系统中，FSSC频率不受任何测试的土壤气候或轮作历史特征的影响，而在常规条件下，它与根腐病发生率和轮作中谷物豆类的较高频率相关。已知这种真菌复合物对豌豆根健康很重要。

and we have no explanation why it did not play a prominent role under organic conditions despite equal isolation frequencies in both systems.

尽管两个系统的隔离频率相同，但我们无法解释为什么它在有机条件下没有发挥突出作用。

Taken together, in all years, several potential pathogens could be found in predominantly asymptomatic pea roots, showing that the

综上所述，多年来，在主要无症状的豌豆根中可以发现几种潜在的病原体，这表明

Fusarium

镰刀菌

and

和

Didymella

spp. associated with peas often reside in the roots without causing substantial damage

与豌豆相关的spp.通常存在于根部而不会造成实质性损害

. The occurrence of such asymptomatic infections is likely the result

。这种无症状感染的发生很可能是结果

of a balanced antagonism between the plants defense mechanisms and the virulence factors of the pathogens. Given that biological interactions are never neutral, we recently showed, for example, that asymptomatic infections with

植物防御机制与病原体毒力因子之间的平衡拮抗作用。鉴于生物相互作用从来都不是中性的，例如，我们最近表明，无症状感染

D. pinodella

D. 皮诺德

can reduce wheat biomass

可以减少小麦生物量

and can also cause severe pre-emergence death and post-emergence root rot in peas

也可能导致豌豆严重的出苗前死亡和出苗后根腐病

. Asymptomatic root infections by

.无症状根感染

D. pinodella

D. 皮诺德

and

和

F. redolens

F. 规律性

have also been linked to reduced faba bean yields

也与蚕豆产量下降有关

, suggesting higher investment of the faba bean to maintain a balanced antagonism with these fungi. The negative correlation of conventional pea yields with members of the FOSC in this study suggests similar underlying interactions. Furthermore, environmental factors and the timing of root infections are important in maintaining balanced antagonism and influence disease development, including the expression of visible disease symptoms.

，表明蚕豆的投资更高，以保持与这些真菌的平衡拮抗作用。在这项研究中，传统豌豆产量与FOSC成员的负相关表明类似的潜在相互作用。此外，环境因素和根部感染的时间对于维持平衡的拮抗作用和影响疾病发展（包括可见疾病症状的表达）很重要。

Fusarium

镰刀菌

and

和

Didymella

spp. are often opportunistic pathogens that can cause damage especially well if pant stress occurs in early crop growth stages, whereas pea can tolerate well root infections in later growth stages

spp.通常是机会性病原体，如果在作物生长早期发生喘息胁迫，会造成特别严重的损害，而豌豆在生长后期可以很好地耐受根部感染

if environmental conditions are not too extreme (e.g. prolonged drought or rainy period). Furthermore, beneficial fungi in the roots may also have played a role in the lack of clear disease symptoms and the weak association between root rot severity and the major fungal species identified in this study e.g.

如果环境条件不太极端（例如长期干旱或雨季）。此外，根中的有益真菌也可能在缺乏明确的疾病症状以及根腐严重程度与本研究中鉴定的主要真菌物种之间的弱关联中起作用。

beneficial .

有益。

F. equiseti

F. 马匹

and arbuscular mycorrhizal fungi

和丛枝菌根真菌

which have the ability to manipulate plant defense and/or pathogen infection sites.

具有操纵植物防御和/或病原体感染部位的能力。

Thus, pedo-climatic factors appeared to be the main drivers for the occurrence of the most common fungal species with clear differences between spring and winter grown peas. The most obvious interactions occurred with soil pH which interacted with the occurrence of certain fungi, especially the FOSC members and .

因此，pedo气候因素似乎是最常见真菌物种发生的主要驱动因素，春季和冬季种植的豌豆之间存在明显差异。最明显的相互作用发生在土壤pH值上，这与某些真菌的发生相互作用，特别是FOSC成员和。

F. tricinctum

F、三角肌

that correlated with reduced or increased soil pH values, respectively. The interactions with cropping history varied depending on the fungal species. Higher frequency of legumes in rotation or shorter intervals between legumes was associated with the presence of

这分别与土壤pH值的降低或增加有关。与种植历史的相互作用因真菌种类而异。豆类轮作频率较高或豆类之间的间隔较短与豆类的存在有关

D. pinodella

D. 皮诺德

and to a lesser extent the FSSC. However, for

以及较小程度的FSSC。但是，对于

F. redolens

F. 规律性

in organic spring peas, the opposite trend was observed. This suggests some specific microbial interactions depending on the species are involved. Only in conventional systems, root health and yields were affected by specific fungal species. Root rot incidence was associated with increased infection rates of .

。这表明一些特定的微生物相互作用取决于所涉及的物种。只有在常规系统中，根系健康和产量才受到特定真菌种类的影响。根腐病发病率与感染率增加有关。

F. redolens

F. 规律性

and members of the FSSC complex. In contrast, yields were negatively correlated with the frequencies of FOSC complex members and positively with

和FSSC复合体的成员。相比之下，产量与FOSC复杂成员的频率呈负相关，与

F. tricinctum

F、三角肌

Materials and methods

材料和方法

Surveys, sampling and disease assessments

调查、抽样和疾病评估

Sample collection, fieldwork and laboratory analyses followed the procedures outlined in Šišić et al. (2022)

样本收集、实地调查和实验室分析遵循西西奇等人（2022年）概述的程序

which were used in parallel survey of faba beans. Between 2016 and 2019, 99 spring and 34 winter pea fields were sampled across Germany (Fig.

用于蚕豆的平行调查。在2016年至2019年期间，在德国各地采样了99个春季和34个冬季豌豆田（图）。

and Supplementary Table

和补充表

). Among the spring pea fields, 23 were managed organically and 76 conventionally. Most winter pea fields were managed organically (29 fields) and only 5 conventionally. Historical cropping data were collected directly from farmers. These included number of times (in years) that fields were planted to various leguminous species (pea, faba bean, lentil, lupin, soybean, clovers and alfalfa, vetch and the unspecified group of ‘other grain’ or ‘small seeded legumes’) and to cereals (aggregated across all cereal types) for 5 and 11 years preceding the sampling.

)。在春季豌豆田中，23个是有机管理的，76个是常规管理的。大多数冬季豌豆田是有机管理的（29块），只有5块是常规管理的。历史种植数据直接从农民那里收集。这些包括在采样前5年和11年内，将田地种植到各种豆科物种（豌豆，蚕豆，扁豆，羽扇豆，大豆，三叶草和紫花苜蓿，野豌豆和未指定的“其他谷物”或“小种子豆科植物”）和谷物（在所有谷物类型中聚集）的次数（以年为单位）。

Spring peas in 8 organic and 3 conventional fields as well as all organic winter peas and two conventional winter pea crops were grown in mixtures with cereals or false flax (.

8个有机田和3个常规田的春豌豆以及全有机冬豌豆和两种常规冬豌豆作物与谷物或假亚麻混合种植（。

Camelina sativa

亚麻荠

) (Supplementary Table

)（补充表

S1级

Fig. 5

图5

Map of Germany showing locations of the surveyed organic and conventional spring and winter pea fields.

德国地图，显示了被调查的有机和传统春季和冬季豌豆田的位置。

Full size image

全尺寸图像

Soil samples were collected in spring from a 0–20 cm depth by taking 20 cores from two randomly selected 5 m

plots in each field, located 10 to 20 m apart. The samples were analyzed for soil pH, sand, silt, clay and soil organic matter content according to the DIN 7025:2018 − 03

每个田地的地块相距10至20米。 − 03

protocol. Meteorological data were obtained from the nearest weather stations which were always located within 10 km of the sampled fields.

协议。气象数据来自最近的气象站，这些气象站总是位于采样场10公里以内。

Root sampling was performed by uprooting 36 to 40 pea plants from each field during full flowering from the same two 5 m² areas used for soil sampling. Half of the roots were immediately washed and assessed for root rot severity using a scoring system ranging from 1 to 9, where a score of 1 represented healthy plants and a score of 9 indicated dying plants.

通过在完全开花期间从每个田地中拔出36至40株豌豆植物，从用于土壤采样的相同的两个5平方米区域进行根采样。立即洗涤一半的根，并使用1至9的评分系统评估根腐严重程度，其中1分表示健康植物，9分表示垂死植物。

(Fig.

（图。

). The other half of the roots was sent to the University of Kassel and preserved at −18 °C until fungal isolations were performed. At pea maturity, fields were visited again and grain yields were determined by hand harvesting 2.5 m² next to the 5 m² areas used for soil and root sampling (as the initial 5 m² area had been disturbed).

)。另一半的根被送到卡塞尔大学，保存在-18°C，直到进行真菌分离。豌豆成熟时，再次访问田地，通过在用于土壤和根系采样的5平方米区域旁边手工收获2.5平方米来确定谷物产量（因为最初的5平方米区域受到干扰）。

Gain yield was adjusted to 86% dry matter before statistical analyses..

在统计分析之前，将增益产量调整为干物质的86%。。

Fig. 6

图6

Root discoloration levels and assigned root rot disease severity ratings (1 = healthy plant to 9 = dying plant, photo credit: Lucas Langanky and Harald Schmidt).

根变色水平和指定的根腐病严重程度等级（1=健康植物至9=垂死植物，照片来源：Lucas Langanky和Harald Schmidt）。

Full size image

全尺寸图像

Fungal isolations, morphological and molecular characterization of isolates

真菌分离，分离物的形态和分子表征

Fungal isolations targeted species within the

真菌分离的目标物种

Fusarium

镰刀菌

and

和

Didymella

genera. Roots were first thoroughly washed in distilled water, surface sterilized using 3% sodium hypochlorite for 10 s and rinsed well in distilled water and placed on filter paper under a laminar flow hood for about 1 h to dry. From each root, three approximately 1-cm-long segments were cut out from the upper, middle and lower portions and placed on Coons media.

属。首先将根在蒸馏水中彻底洗涤，使用3%次氯酸钠表面灭菌10秒，并在蒸馏水中充分冲洗，并在层流罩下放置在滤纸上约1小时以干燥。从每个根部，从上部，中部和下部切下三个约1厘米长的部分，并放置在Coons培养基上。

for incubation at 20˚C under a 12-hour light/dark cycle and black-light blue light. After an incubation period of 1 to 2 weeks, fungal colonies that developed from the root segments were sub-cultured separately into Petri dishes containing half-strength potato dextrose agar (19 g/l Difco PDA and 10 g/l agar).

用于在20℃下在12小时光照/黑暗循环和黑光-蓝光下孵育。孵育1至2周后，将从根段发育的真菌菌落分别传代培养到含有半强度马铃薯葡萄糖琼脂（19 g/l Difco PDA和10 g/l琼脂）的培养皿中。

Pure cultures were generated either through hyphal tipping for .

纯培养物是通过菌丝倾斜产生的。

Fusarium

镰刀菌

species or by transferring individual pycnidia for

物种或通过转移个体pycnidia

Didymella

species. The obtained isolates were identified to the species level based on their cultural characteristics and the morphology of conidiogenous cells

物种。根据其培养特性和分生孢子细胞的形态，将获得的分离株鉴定为物种水平

Molecular confirmation of 124

124的分子确认

Fusarium

镰刀菌

and 25

和25

Didymella

isolates representing 14 different fungal species was carried out by sequencing the translation-elongation factor 1 alpha (

通过对翻译延伸因子1α进行测序，分离出代表14种不同真菌的菌株(

tef1

) locus for

)的轨迹

Fusarium

镰刀菌

spp. and the β tubulin (

β 管素（英语：β tubulin）

tub2

tub2型

) for

)对于

Didymella

spp. (Supplementary Table

物种（补充表

S4级

)

. Genomic DNA was extracted from pure cultures grown on half-strength PDA (

.从半强度PDA上生长的纯培养物中提取基因组DNA(

Fusarium

镰刀菌

spp.) and on Coons medium (

和Coons培养基(

Didymella

spp.), following the method described by Doyle and Doyle (1987)

遵循Doyle和Doyle（1987）描述的方法

. The

.The

tef1

gene was amplified using primers EF1 (5′ ATG GGT AAG GARG ACA AGA C 3′) and EF2 (5′ GGA RGT ACC AGT SAT CAT GTT 3′)

使用引物EF1（5'ATG GGT AAG GARG ACA AGA C 3'）和EF2（5'GGA RGT ACC AGT SAT CAT GTT 3'）扩增基因

, and the

，以及

tub2

tub2型

region was amplified with primers Btub2Fd (5′ GTB CAC CTY CAR ACC GGY CAR TG 3′) and Btub4Rd (5′ CCR GAY TGR CCR AAR ACR AAG TTG TC3′)

. The amplified products were visualized through electrophoresis on a 1% agarose gel and then purified using the DNA Clean & Concentrator kit (Zymo Research, Freiburg, Germany) according to the manufacturers guidelines. Sanger sequencing was conducted in both directions by Macrogen Europe Laboratories (Amsterdam, Netherlands).

通过在1%琼脂糖凝胶上电泳使扩增产物可视化，然后根据制造商的指南使用DNA Clean＆Concentrator试剂盒（Zymo Research，弗莱堡，德国）进行纯化。Sanger测序由Macrogen Europe Laboratories（荷兰阿姆斯特丹）在两个方向上进行。

The raw sequence data were assembled and any errors were manually corrected using SeqMan Lasergene software (DNAStar, Madison, WI, U.S.A.). Generated sequences were then used as queries for the Fusarium-ID v. 1.0.

组装原始序列数据，并使用SeqMan Lasergene软件（DNAStar，麦迪逊，威斯康星州，美国）手动校正任何错误。然后将生成的序列用作镰刀菌ID v.1.0的查询。

and NCBI

关于NCBI

databases to verify the taxonomic identity of the isolates.

数据库以验证分离株的分类学身份。

In addition, single-locus phylogenetic analyses were conducted using

此外，使用

tef1

gene sequences generated for 30 isolates of the

为30个分离株产生的基因序列

Fusarium solani

茄病镰刀菌

species complex (FSSC) and 17 isolates of the

物种复合体（FSSC）和17个分离株

Fusarium oxysporum

Fusarium oxysporum（英语：Fusarium oxysporum）

species complex (FOSC). Reference sequences (Supplementary Table

物种复合体（FOSC）。参考序列（补充表

S5级

and Supplementary Table

和补充表

S6级

) for these analyses were sourced from previously published phylogenetic studies on the FSSC and the FOSC

)这些分析来源于先前发表的关于FSSC和FOSC的系统发育研究

complexes. Representative isolates from the most recent studies on pea and faba bean root rots conducted in the UK, France and Germany

复合物。在英国、法国和德国进行的最新豌豆和蚕豆根腐病研究中的代表性分离株

were also included. The final datasets consisted of 126

也包括在内。最终的数据集包括126个

tef1

sequences of the FSSC and 210 of the FOSC (Supplementary Table

FSSC的序列和FOSC的210（补充表

S5级

and Supplementary Table

和补充表

S6级

). Sequence alignments were generated using MAFFT v.7

)。序列比对是使用MAFFT v.7生成的

and were further adjusted manually with MEGA v6

并使用MEGA v6进行了进一步的手动调整

. A Maximum-Likelihood (ML) analysis was conducted with RAxML-VI-HPC v. 7.0.3, employing non-parametric bootstrapping with 1000 replicates via the Cipres portal

。使用RAxML VI HPC v.7.0.3进行了最大似然（ML）分析，通过Cipres门户使用了1000个重复的非参数自举

. For outgroup purposes,

.出于外群目的，

F. udum

F.udum

(CBS 177.31) and

（CBS 177.31）和

F. thapsinum

F. 日期

(H05-557 S-1 DCPA) were used (Supplementary Table

（H05-557 S-1 DCPA）被使用（补充表

S5级

and Supplementary Table

和补充表

S6级

). The resulting phylogenetic trees were visualized and edited in FigTree (version 1.4.4;

)。由此产生的系统发育树在FigTree（版本1.4.4）中可视化和编辑；

http://tree.bio.ed.ac.uk/software/figtree/

) and Adobe Illustrator CS5.1

)和Adobe Illustrator CS5.1

Data analyses

数据分析

All statistical analyses were conducted in R

所有统计分析均在R中进行

. Isolation frequencies (% colonized roots) were calculated by dividing the number of roots containing a species by the total number of roots processed. Additionally, if the mean disease severity score within a given field was greater than 3, the field was considered to be seriously affected, a condition that was assessed as the incidence on the field level.

.分离频率（%定殖根）通过将含有物种的根数除以处理的根总数来计算。此外，如果给定领域内的平均疾病严重程度评分大于3，则该领域被认为受到严重影响，这种情况被评估为现场水平的发病率。

. The data collected from conventional winter pea fields are presented, however, these data were not included in statistical analyses due to the limited sample size (only 5 fields).

。提供了从传统冬季豌豆田收集的数据，但是，由于样本量有限（只有5个田），这些数据未包括在统计分析中。

Root rot severity data were analyzed with non-parametric Kruskal-Wallis tests with the pea type (spring vs winter pea), management system (organic vs conventional), sowing pattern (pure vs mixed stands for spring pea only) and year as main factors. Kruskal multiple comparison tests were performed in case of significant effects.

采用非参数Kruskal-Wallis检验分析了豌豆类型（春豌豆与冬豌豆），管理系统（有机与常规），播种方式（仅春豌豆纯林与混交林）和年份的根腐严重程度数据。在显着影响的情况下进行Kruskal多重比较测试。

Benjamini and Hochberg.

Benjamini和Hochberg。

stepwise adjustment controlled false discovery rates (FDR) and reduced type I errors. For the isolation frequency data, rare species (< 2% of total root colonization rates) were excluded from the analysis. Generalized linear mixed models with management system, pea type (spring vs winter pea), sowing pattern (pure vs mixed stands for organic spring pea only) and sampling year as factors were employed on proportional data with a binomial response and logit link function.

逐步调整控制错误发现率（FDR）并减少I型错误。对于分离频率数据，分析中排除了稀有物种（占总根定殖率的2%）。以管理系统，豌豆类型（春季与冬季豌豆），播种模式（纯林与混交林仅用于有机春豌豆）和采样年份为因素的广义线性混合模型用于具有二项式响应和logit链接函数的比例数据。

. Fields were modeled as random effects, accounting for nested sampling replicates within each field. Model goodness was assessed using Pearson chi-square residual tests, normality checks, and outlier detection (package ‘DHARMa’

。使用Pearson卡方残差检验，正态性检验和异常值检测（软件包“DHARMa”）评估模型的优度

. Significant main effects were evaluated with ANOVA and Tukey’s correction for post hoc comparisons (

。通过ANOVA和Tukey校正评估了显着的主要影响，以进行事后比较(

< 0.05) (package ‘lsmeans’

<0.05）（包“lsmeans”

To explore the relationship between the frequencies of the eight most commonly isolated fungal species and yield, root rot incidence on the field level, cropping histories and pedo-climatic factors, Pearson correlation analysis was employed (package ‘Hmisc’

为了探讨8种最常见的真菌种类的频率与产量、田间根腐病发生率、种植历史和土壤气候因素之间的关系，采用Pearson相关分析（Hmisc软件包）

. Only statistically significant (p < 0.05) correlation coefficients of ≥ ± 0.30 are reported. In addition, to provide an overview of the soil types for the sampled fields, we employed hierarchical clustering on principal components (HCPC) using the ‘FactoMineR’ package

。仅报告统计学显着性（p<0.05）相关系数≥0.30。此外，为了概述采样场的土壤类型，我们使用“FactoMineR”软件包对主成分（HCPC）进行了层次聚类

. This approach involves grouping of the fields into clusters based on similarities in soil abiotic properties namely, sand, silt, clay, organic matter content and pH. The R packages ‘maps’

这种方法涉及根据土壤非生物特性的相似性将田地分组，即沙子、淤泥、粘土、有机质含量和pH值。R软件包“地图”

, ‘raster’

，“光栅”

and ‘ggplot2’

和“ggplot2”

were used to show the coordinates of surveyed fields on a map of Germany. The ggplot2 visualizations were further enhanced with R package ‘ggsn’

被用来在德国地图上显示被调查领域的坐标。使用R包“ggsn”进一步增强了ggplot2的可视化

which was used to add scale bars and north arrows to the map.

用于向地图添加比例尺和北箭头。

Data availability

数据可用性

All data are included within the article and its supplementary materials. The complete raw data set generated during this study is available in Supplementary Table S1. Data can also be obtained from the corresponding author upon reasonable request.

所有数据均包含在文章及其补充材料中。本研究期间生成的完整原始数据集可在补充表S1中找到。。

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Acknowledgements

致谢

This work was carried out within the framework of the research projects PATHO-ID (2814EPS40) and APSOLU (2814EPS035), funded by the German Federal Ministry of Food and Agriculture within the framework of the BMEL protein plant strategy, in cooperation with the German Demonstration network Pea/Bean.

这项工作是在研究项目PATHO-ID（2814EPS40）和APSOLU（2814EPS035）的框架内进行的，该项目由德国联邦食品和农业部在BMEL蛋白质植物战略的框架内与德国示范网络Pea/Bean合作资助。

Author information

作者信息

Authors and Affiliations

作者和隶属关系

Section of Ecological Plant Protection, University of Kassel, 37213, Witzenhausen, Germany

卡塞尔大学生态植物保护科，37213，德国威岑豪森

Adnan Šišić, Jelena Baćanović-Šišić & Maria R. Finckh

Adnan Šišić、Jelena Baćanović-Šišić 和 Maria R. Finckh

Foundation Ecology & Agriculture (SOEL), 53474, Ahrweiler, Germany

生态与农业基金会（SOEL），53474，德国Ahrweiler

Harald Schmidt

哈拉德·施密特

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叶琳娜·巴察诺维奇-西西奇

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Contributions

捐款

A.Š., H.S., J.B.Š., M.F study design/methodology/investigation. A.Š. analyzed the results, prepared data presentation and drafted the manuscript. A.Š., H.S., M.F resources/funding acquisition. All authors discussed results, revised the manuscript and approved the submitted version.

A、 Š。，H、 S.，J.B.Š。，M、 F研究设计/方法/调查。A、 Š。分析结果，准备数据展示并起草手稿。A、 Š。，H、 S.，M.F资源/资金收购。所有作者都讨论了结果，修改了稿件并批准了提交的版本。

Corresponding author

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Adnan Šišić

阿德南西西奇

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道德宣言

Competing interests

相互竞争的利益

The authors declare no competing interests.

作者声明没有利益冲突。

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其他信息

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出版商注释

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Electronic supplementary material

电子补充材料

Below is the link to the electronic supplementary material.

以下是电子补充材料的链接。

Supplementary Material 1

补充材料1

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权限和权限

Open Access

开放存取

This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material.

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You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

To view a copy of this licence, visit .

要查看此许可证的副本，请访问。

http://creativecommons.org/licenses/by-nc-nd/4.0/

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重印和许可

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关于本文

Cite this article

引用本文

Šišić, A., Baćanović-Šišić, J., Schmidt, H.

Šišić， A.， Baćanović-Šišić， J.， Schmidt， H.

et al.