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氨基乙氧基乙烯基甘氨酸和低氧控制的“Gala”苹果贮藏转移功能微生物群


来源: Connor Lane et al  发布日期: 2023-09-12  访问量: 239


采后微生物群落的复杂性和相互关联的动态需要对整个微生物组进行表征,以充分了解病原体、生物防治和果实质量之间的关系。本研究研究了采前植物生长调节剂氨基乙氧基乙烯基甘氨酸(AVG,0.25 g L−1)抑制乙烯生产,以及与空气储存相比的低O2(0.5%和2%)控制气氛(CA)储存对在0.5°C下储存的“Gala”苹果表面微生物组的影响
标签: 氨基乙氧基乙烯基甘氨酸、低氧、动态气调、微生物群、DCA
 

Aminoethoxyvinylglycine and low oxygen controlled atmosphere storage shift functional microbiomes of ‘Gala’ apples

氨基乙氧基乙烯基甘氨酸和低氧控制的“Gala”苹果贮藏转移功能微生物群
Connor Lane,Yosef Al Shoffe,Jenny Kao-Kniffin,Christopher B. Watkins


    Horticulture Section, School of Integrative Plant Science, College of Agriculture and Life Sciences, Cornell University, Ithaca, NY 14853, USA
Received 17 May 2023, Revised 17 August 2023, Accepted 21 August 2023, Available online 28 August 2023, Version of Record 28 August 2023.
https://doi.org/10.1016/j.postharvbio.2023.112546

 

Abstract

The complexity and interconnected dynamics of postharvest microbial communities require whole-microbiome characterization to fully understand relationships among pathogens, biocontrol, and fruit quality. This study investigated the effects of the preharvest plant growth regulator aminoethoxyvinylglycine (AVG, 0.25 g L−1), which inhibits ethylene production, and low O2 (0.5 % and 2 %) controlled atmosphere (CA) storage compared with air storage, on the surface microbiome of ‘Gala’ apples stored at 0.5 °C. AVG and low O2 concentrations affected bacterial but not fungal communities. Bacterial but not fungal diversity decreased after 9 months of CA storage. Microbial genera with potential biocontrol functions such as Pseudomonas and Aureobasidium were found across all time points and treatments. The microbiomes detected in CA stored fruit were the most different from those in air stored fruit late in storage. At this time, metagenome prediction methods found that low O2 fruit may harbor bacteria with fewer gene pathways using O2 as a reactant compared to fruit in air storage. The results indicate that storage conditions influence the composition, diversity, and function of microbiomes inhabiting fruit surfaces, which provide a greater basis for understanding biocontrol and pathogen population dynamics in a more holistic manner.

采后微生物群落的复杂性和相互关联的动态需要对整个微生物组进行表征,以充分了解病原体、生物防治和果实质量之间的关系。本研究研究了采前植物生长调节剂氨基乙氧基乙烯基甘氨酸(AVG,0.25 g L−1)抑制乙烯生产,以及与空气储存相比的低O2(0.5%和2%)控制气氛(CA)储存对在0.5°C下储存的“Gala”苹果表面微生物组的影响。AVG和低O2浓度影响细菌群落,但不影响真菌群落。CA贮藏9个月后,细菌而非真菌的多样性降低。在所有时间点和处理中都发现了具有潜在生物控制功能的微生物属,如假单胞菌和Aureobasidium。CA贮藏果实中检测到的微生物群与空气贮藏后期果实中检测的微生物群差异最大。此时,宏基因组预测方法发现,与空气中储存的水果相比,低O2水果可能含有使用O2作为反应物的基因途径较少的细菌。结果表明,贮藏条件会影响果实表面微生物群的组成、多样性和功能,这为更全面地了解生物控制和病原体种群动态提供了更大的基础。


Introduction

Postharvest decay is an important issue for horticultural industries due to economic losses and health concerns from mycotoxins (Bruton, 1994, Hua et al., 2018, Patriarca, 2019). With the advance of Next-Generation Sequencing, it is possible to study these pathogens in greater detail due to whole community profiling that contextualizes the nature of pathogen colonization and persistence with respect to other microorganisms (Cao et al., 2017). Community profiling through amplicon sequencing is particularly well-equipped for providing the ecological context of biocontrol action, as microbe-microbe interactions can be characterized for the vast array of microorganisms on fruit surfaces (Droby and Wisniewski, 2018). Indeed, host and microbiome functions are so intertwined that some argue that they can be viewed as a single unit called a “holobiont” (Gordon et al., 2013), which is an important framework in postharvest microbiology due to delineation of the multitude of interconnected systems involving plant and microbial physiology (Droby et al., 2022, Wisniewski and Droby, 2019). The idea of an interconnected system between host and microbe is supported by cultivar-specific microbiomes in apples that indicate possible host-microbe co-evolution (Abdelfattah et al., 2021b, Liu et al., 2018). Knowledge about postharvest microbiome assembly and function could lead to a more comprehensive understanding of how pathogens and biocontrol dynamics can contribute to resilient food systems.

由于真菌毒素造成的经济损失和健康问题,收获后腐烂是园艺行业的一个重要问题(Bruton,1994,Hua等人,2018,Patriarca,2019)。随着下一代测序的进展,由于整个群落的特征分析,病原体定殖的性质和相对于其他微生物的持久性,因此有可能对这些病原体进行更详细的研究(Cao et al.,2017)。通过扩增子测序进行的群落分析特别适合提供生物控制作用的生态环境,因为可以对水果表面的大量微生物进行微生物-微生物相互作用的表征(Droby和Wisniewski,2018)。事实上,宿主和微生物组的功能是如此交织在一起,以至于一些人认为它们可以被视为一个被称为“全生物”的单一单元(Gordon et al.,2013),这是采后微生物学的一个重要框架,因为它描绘了涉及植物和微生物生理学的众多相互关联的系统(Droby et al.,2022,Wisniewski和Droby,2019)。宿主和微生物之间相互连接系统的想法得到了苹果中品种特异性微生物群的支持,这些微生物群表明宿主-微生物可能共同进化(Abdelfattah等人,2021b,Liu等人,2018)。了解采后微生物组的组装和功能,可以更全面地了解病原体和生物控制动态如何有助于建立有弹性的食物系统。

Apples are an ideal system for investigation of the surface microbiome due to the variety of conditions that influence postharvest physiology which can be linked with microbiome shifts. Apples include a large number of cultivars with long growing seasons, a variety of preharvest management practices, postharvest treatments, and storage under air or controlled atmosphere (CA) conditions for extended time periods. Factors such as growing region and organic vs conventional management have revealed compositional differences of the microbiome (Abdelfattah et al., 2016, Abdelfattah et al., 2021a, Leff and Fierer, 2013, Shen et al., 2022, Vepštaitė-Monstavičė et al., 2018, Wassermann et al., 2019b). Biotic factors such as the application of biocontrol agents can shift the entire microbiome composition in addition to controlling specific pathogens (Biasi et al., 2021, Shi et al., 2022). Pre- and postharvest treatments including hot water treatments and postharvest washing and waxing affect microbial community composition (Abdelfattah et al., 2020, Bösch et al., 2021, Shen et al., 2018, Wassermann et al., 2019a). Altogether, the findings reveal that apple microbiomes are both influenced by many common factors, and that a “core” apple microbiome exists. Common microbial taxa have been found in apples worldwide (Abdelfattah et al., 2021a), and many studies share similar high-abundance genera with potential biocontrol function, such as the Aureobasidium fungi and the Pseudomonas bacteria (Mari et al., 2012, Scherwinski et al., 2008). The relative consistency of the apple microbiome and the potential to manipulate its composition and function make it an excellent system for applying ecological strategies to food systems.

苹果是研究表面微生物组的理想系统,因为影响采后生理的条件多种多样,这可能与微生物组的变化有关。苹果包括大量生长季节长的品种、各种采前管理方法、采后处理以及在空气或受控大气(CA)条件下长时间储存。生长区域和有机管理与传统管理等因素揭示了微生物组的组成差异(Abdelfattah等人,2016,Abdelfatta等人,2021a,Leff和Fierer,2013,Shen等人,2022,Vepštaitë-Monstavičõ等人,2018,Wassermann等人,2019b)。生物因素,如生物控制剂的应用,除了控制特定病原体外,还可以改变整个微生物组的组成(Biasi等人,2021,Shi等人,2022)。采前和采后处理,包括热水处理、采后清洗和打蜡,会影响微生物群落组成(Abdelfattah等人,2020,Bösch等人,2021,Shen等人,2018,Wassermann等人,2019a)。总之,研究结果表明,苹果微生物组受到许多共同因素的影响,并且存在“核心”苹果微生物组。世界各地的苹果中都发现了常见的微生物类群(Abdelfattah等人,2021a),许多研究共享具有潜在生物控制功能的类似高丰度属,如Aureobasidium真菌和假单胞菌(Mari等人,2012,Scherwinski等人,2008)。苹果微生物组的相对一致性以及操纵其组成和功能的潜力使其成为将生态策略应用于食品系统的优秀系统。

Apples are a climacteric fruit, producing ethylene that modulates the ripening process (Johnston et al., 2009). Depending on the growing region, preharvest treatments with the plant growth regulators (PGRs) aminoethoxyvinylglycine (AVG; commercial formulation ReTain™) or 1-methylcycopropene (1-MCP; commercial formulation Harvista®) are applied to manage the harvest in many fruit growing regions (Watkins, 2017). AVG inhibits the activity of 1-aminocyclopropane-1-carboxylate (ACC) synthase (ACS) by binding to pyridoxal-5′-phosphate. ACS catalyzes the conversion of methionine to ACC, the precursor to ethylene in the ethylene biosynthetic pathway (Boller et al., 1979), although its effects on non-ethylene pathways (Le Deunff et al., 2019) cannot be excluded. 1-MCP inhibits ethylene perception (Sisler, 2006). Regardless of action, the PGRs can reduce fruit losses due to preharvest drop and delay harvest to allow fruit size to increase (Al Shoffe et al., 2021, Arseneault and Cline, 2016, Doerflinger et al., 2019, Greene and Schupp, 2004, Watkins, 2008, Yuan and Li, 2008).

苹果是一种周期性水果,产生调节成熟过程的乙烯(Johnston等人,2009)。根据生长区域的不同,用植物生长调节剂(PGRs)氨基乙氧基乙烯基甘氨酸(AVG)进行采前处理;商业配方ReTain™) 或1-甲基椰菜红素(1-MCP;商业配方Harvista®)用于管理许多水果种植区的收成(Watkins,2017)。AVG通过与吡哆醛-5′-磷酸结合抑制1-氨基环丙烷-1-羧酸合酶(ACS)的活性。ACS催化甲硫氨酸转化为ACC,ACC是乙烯生物合成途径中乙烯的前体(Boller等人,1979),尽管不能排除其对非乙烯途径的影响(Le Deunff等人,2019)。1-MCP抑制乙烯感知(Sisler,2006)。无论采取何种行动,PGR都可以减少因采前下降而造成的水果损失,并推迟收获,以使水果大小增加(Al-Shoffe等人,2021,Arseneault和Cline,2016,Doerflinger等人,2019,Greene和Schupp,2004,Watkins,2008,Yuan和Li,2008)

No studies to date have investigated the effects of ethylene inhibitors on the apple surface microbiome, although other work has linked ethylene inhibitors to the microbiomes of pear and kiwifruit (Xie et al., 2021, Zhang et al., 2021). Ethylene is known to mediate plant-microbe interactions, such as working with jasmonic acid to increase defense against necrotrophs but it inhibits the ability of salicylic acid to activate defenses against biotrophs (Adie et al., 2007). The relationship may act in both directions, with plant microbiomes mediating host microbiome signaling (Gamalero and Glick, 2015, Ravanbakhsh et al., 2018). Also, certain bacterial and fungal pathogens are able to use ethylene as a virulence factor to aid in colonization plant tissues (van Loon et al., 2006), highlighting the importance of ethylene in microbial signaling as well as plant signaling.

迄今为止,没有研究调查乙烯抑制剂对苹果表面微生物组的影响,尽管其他研究将乙烯抑制剂与梨和猕猴桃的微生物组联系起来(Xie等人,2021,Zhang等人,2021)。众所周知,乙烯可以介导植物与微生物的相互作用,例如与茉莉酸协同作用以增强对坏死营养因子的防御,但它会抑制水杨酸激活对生物营养因子防御的能力(Adie等人,2007)。这种关系可能双向作用,植物微生物组介导宿主微生物组信号传导(Gamalero和Glick,2015,Ravanbakhsh等人,2018)。此外,某些细菌和真菌病原体能够利用乙烯作为毒力因子来帮助植物组织定植(van Loon等人,2006),这突出了乙烯在微生物信号和植物信号中的重要性。

Short-term air storage of apples is common, but maintenance of quality during long-term storage is reliant on the use of standard controlled atmosphere (CA) storage, which is based on low O2 (1–3 %), and elevated CO2 (0.5–5 %) concentrations, with specific recommendations depending on the cultivar (Watkins, 2017). More recently, the adoption of dynamic CA (DCA) based on monitoring fruit to avoid low O2 stress has allowed storage of fruit at concentrations that are close to the anaerobic compensation point (Bessemans et al., 2016, Thewes et al., 2020, Zanella and Rossi, 2015). Positive results with DCA in New York State have led to the adoption of 0.5 % O2 for ‘Gala’ without use of sensing equipment. In addition to reducing respiration, low O2 maintains quality by reducing ethylene production and its perception by the fruit, thereby slowing ripening. It has long since been established that CA storage can slow the growth of certain pathogens in apples (Reichel, 1974, Schulz, 1974), and CA can also mediate biocontrol-pathogen interactions, reducing biocontrol efficacy at 1 % O2 compared with 3 % O2 (Usall et al., 2000). Additionally, compared with apples at the time of harvest, a number of different pathogen control techniques were less effective after apples were stored in CA (de Capdeville et al., 2002). Apples stored in CA consistently have different microbiomes than those stored in cold air across multiple years (Bösch et al., 2021), but the effects of specific O2 concentrations such as 0.5 % compared with 2 % on the fruit microbiome is unknown.
苹果的短期空气储存很常见,但在长期储存过程中质量的保持取决于标准控制气氛(CA)储存的使用,该储存基于低O2(1-3%)和高CO2(0.5-5%)浓度,具体建议取决于品种(Watkins,2017)。最近,采用基于监测水果以避免低O2胁迫的动态CA(DCA),使水果的储存浓度接近厌氧补偿点(Bessemans等人,2016,Thewes等人,2020,Zanella和Rossi,2015)。纽约州DCA的积极结果导致“Gala”在不使用传感设备的情况下采用0.5%的O2。除了减少呼吸外,低O2还通过减少乙烯的产生和果实对乙烯的感知来保持品质,从而减缓成熟。长期以来,人们已经确定,CA储存可以减缓某些病原体在苹果中的生长(Reichel,1974,Schulz,1974),CA还可以介导生物防治病原体的相互作用,与3%O2相比,在1%O2下降低生物防治效果(Usall等人,2000)。此外,与收获时的苹果相比,将苹果储存在CA后,许多不同的病原体控制技术效果较差(de Capdeville等人,2002)。储存在CA中的苹果与储存在冷空气中的苹果多年来一直具有不同的微生物组(Bösch等人,2021),但特定O2浓度(如0.5%和2%)对水果微生物组的影响尚不清楚。


The objectives of this investigation were to investigate the effects of AVG as well as CA storage on the microbiome of apple fruit. It was hypothesized that: 1. AVG would alter the composition and function of the surface microbiomes due to ethylene mediating plant-microbe interactions and being produced by certain microbiomes and 2. CA conditions would create a different microbiome than in air storage, and these effects would be more pronounced at lower concentrations of O2. It was also predicted that these shifts would be mirrored by changes in the gene pathways of the microbial community found using metagenomic prediction.

本研究的目的是研究AVG和CA储存对苹果果实微生物组的影响。假设:1。AVG会改变表面微生物组的组成和功能,这是由于乙烯介导植物与微生物的相互作用,并由某些微生物组和2产生。CA条件会产生与空气储存不同的微生物组,并且在较低浓度的O2下,这些影响会更明显。还预测,这些变化将通过宏基因组预测发现的微生物群落基因途径的变化来反映。

 


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