Citrus Fruit Loss Caused by Pathogens

Version	Summary	Created by	Modification	Content Size	Created at	Operation
1		Sarana Rose Sommano	--	3512	2022-08-30 05:54:47	\|
2	format correct	Vivi Li	+ 37 word(s)	3549	2022-08-31 03:21:54	\|

This entry is adapted from the peer-reviewed paper 10.3390/horticulturae8080748

The Sustainable Development Goals (SDGs) contribute to the improvement of production and consumption systems, hence, assisting in the eradication of hunger and poverty. As a result, there is growing global interest in the direction of economic development to create a zero-waste economy or circular economy. Citrus fruits are a major fruit crop, with annual global production surpassing 100 million tons, while orange and tangerine production alone account for more than half of the overall production. During pre- and postharvest stages of citrus fruit production, it is estimated that more than 20% of fruit biomass is lost, due, primarily, to biotic stresses. Due to substantial changes in fruit characteristics and environmental conditions, some of the most economically significant pathogens infect fruits in the field during the growing season and remain dormant or inactive until they resume growth after harvest.

antifungal properties by-products citrus essential oils fruit drop fruit wax greening pectin

1. Introduction

The Sustainable Development Goals (SDGs) of the United Nations aim at sustaining the well-being of the global population and preserving the environment due to the concerns of climate change and the scarcity of natural resources by 2030. The agenda advocates for a new paradigm of growth, in which economic and social development ensure sustainability ^[1]. Among all others, SDG 12 addresses sustainable consumption, the need to enhance resource use efficiency and reduce food loss by recycling and reusing ^[2]. This goal, as do other SDGs, such as Zero Hunger (SDG 2) and No Poverty (SDG 1), contributes to better production and consumption systems that contribute to the eradication of hunger and poverty ^[3]. As a result, scholars, policymakers, and practitioners throughout the world are increasingly interested in the path of economic development and enabling cyclical thinking toward developing a zero-waste economy or circular economy (CE) ^[4]. CE is an economic system in which the concept of end-of-life is substituted by reduce, reuse, recover, and recycle within the production line ^[5]. In recent years, the food industry has taken a number of steps to deal with issues, such as food waste and loss, food safety, production traceability, product quality, and environmental harm ^[6]. The reduction in food waste or agricultural biomass is one of the most critical sustainability issues for food and agricultural producers ^[7]. The value recovery process is an essential component in food supply chain circular movements ^[8]. In line with the CE principle, food biomass is now regarded as a resource for bioproducts, such as active ingredients, enzymes, and organic acids, along with energy and water through biorefinery approaches ^[8]. However, stakeholders across the value chain, from product design to production and distribution to waste disposal, must appreciate the advantages of using biomass ^[7]^[9].

Citrus production has exceeded 140 million tons per year globally, with orange and tangerine production alone accounting for more than half of the total volume ^[10]^[11]^[12]. Commercial citrus production has been recorded by the Food and Agriculture Organization ^[10] in over 100 different countries, across all regions in the tropical and subtropical areas that serve the demand, mainly for fresh consumption ^[10]^[13]. A tremendous amount of money is lost annually due to fruit drop, which occurs during the flowering stage and continues till harvesting. Fruit drop is caused by various biotic and abiotic factors ^[14]^[15]. Abscission is a physiological process that is active and involves the breakdown of cell walls at specific locations, called abscission zones, which are frequently related to stress (i.e., salinity and pathogens causes diseases) and senescence ^[16]. Three waves of abscission are known during fruit production. The first wave is generally at the blooming stage, causing high abscission in buds, flowers, and ovaries ^[17]. After fertilization fails, the second wave emerges, following competition for nutrition (both among fruitlets and between fruitlets and vegetative shoots) and failure of embryo development, and the third wave mainly contributes to losses in fruit drop occurrence ^[16]^[17]. More importantly, plant diseases, such as stem end rot and post-bloom fruit drop, are the primary biotic causes of loss in the orchard during pre-harvesting, with an estimated total loss of fruits of about 20% in the overall output yield ^[18]^[19]^[20]. While the effects of abiotic stresses (i.e., salt and heat stress) on fruit drop have been thoroughly explored ^[21]^[22]^[23], the influence of pathogen-caused disease has not been the subject of a collective review. After harvesting, fresh citrus fruits require standards of quality; therefore, “cosmetic thresholds”, especially from pests and postharvest diseases, were devised ^[24]. Premature fruit drops are the major loss in orchards and farmers usually let them decompose naturally due to high management costs ^[25]. The accumulation of such waste is known to be the cause of disease pathogens in the orchard, which are difficult to eliminate and even cost more for maintenance. Postharvest losses due to fungal and microbial invasion account for up to 35% of total losses, with the most common diseases being caused by green mold, blue mold (Penicillium spp.), and sour rot (Geotrichum candidum) ^[26]. Moreover, fruit rot diseases are responsible for a variety of fungi, including Penicillium, Alternaria, Aspergillus, Colletotrichum, Botryodiplodia, and Phomopsis ^[27].

2. Citrus Pre-Harvest Losses

2.1. Gum Diseases of Citrus Trees Caused by Phytophthora spp. Infection

All commercial citrus scion cultivars are vulnerable to Phytophthora spp. Infection; however, when grafted onto certain rootstocks, they become moderately susceptible to bark infection ^[28]. These pathogens cause yield losses worldwide, especially in susceptible rootstocks in citrus plants, thereby causing considerable concern among growers ^[29]^[30]. Cankers and gum appear on the trunks and main branches of several citrus cultivars, indicating the presence of the disease (Table 1). These cankers girdled the tree’s limbs and trunk, often resulting in the tree’s demise. Cankers are visible in some situations, but only have minor external symptoms in others, and it is only after the outer bark is removed that significant necrotic areas are discovered. Cracks in the bark of affected trees frequently discharge a pale-yellow gum. Though a fungus complex has been linked to Rio Grande gummosis, its etiology is unknown ^[31]. Phytophthora spp. has been identified as harmful to citrus, causing a variety of diseases that affect the roots, trunk, branches, fruits, and shoots ^[32]. In Mediterranean regions, P. citrophthora causes gummosis and root rot and is the most common cause of brown rot. Phytophthora spp. is widely found in citrus soils, causing fibrous root deterioration in susceptible rootstocks, as well as lesions on structural roots and crown rot ^[33]. P. citrophthora attacks aerial plant parts more frequently than P. parasitica and also produces brown rot, a disease that affects fruits, causing a firm light-brown decay, and finally, fruit fall. The reason for this is because P. parasitica does not produce aerial sporangia but P. citrophthora and other species do. Therefore, a citrus tree is more susceptible to P. citrophthora than any Phytophthora spp. ^[34].

2.2. Citrus Greening Disease

Huanglongbing (HLB), also known as citrus greening disease, is the most serious citrus disease in areas where both the disease and its vector are present, primarily in Southeast Asia, India, and South Africa ^[35]. The term “Huanglongbing” is a Chinese term that translates as “yellow dragon disease”, referring to the disease’s symptoms, which include prominent yellow shoots. This disease is caused by a Gram-negative bacterium called Candidatus Liberibacter (Ca. L.) and is spread through natural vectors, such as the psyllids, Trioza erytrea, and Diaphorina citri ^[36]^[37]. This disease has been classified into three subtypes. The first type is Asiatic and it is associated with Ca. L. asiaticus ^[38]. Second, there is an African form associated with Ca. L. africanus ^[32]. Finally, there is an American form, associated with Ca. L. americanus ^[36]^[37]^[39]. The three strains of Ca. L. exhibit distinct temperature responses. The asiaticus is a thermo-tolerant species that can tolerate temperatures above 30 °C, whereas the africanus is thermolabile and prefers temperatures between 22 and 25 °C ^[37]. For the americanus, it, nonetheless, prefers lower temperatures between 17 and 27 °C ^[40].

Symptoms include asymmetrical mottling of the leaves and frequently yellowed midribs. Sectors of the canopy decline and dieback first, followed by the canopy as a whole declining and dying. Once the tree is nearly completely infected, yellow shoots will appear. Symptomatic fruits are lobbed, frequently contain aborted seeds, and have an unpleasant flavor. Fruit production is decreased, symptomatic fruits are small, and symptomatic fruits frequently drop prematurely. Over a period of two to three years, the tree deteriorates and eventually dies ^[36]. The nature of the disease occurs as a result of pathogens penetrating the phloem and attacking the vascular system, clogging the veins and significantly impairing water and nutrient transport ^[37]. Current management strategies are aimed at eradicating vectors, preventing infection spread, and managing infected trees. Individual or combined approaches will have varying degrees of success, depending on the severity of the infestation. The most frequently used practices are preventing infection spread through tree removal, protecting grove edges through intensive monitoring, pesticide use, and biological control of the vector ^[41]. According to Lee ^[36], to assure the production of healthy plants and the prevention of the spread of contaminated nursery stock, HLB control involves quarantine, clean stock, and certification procedures. Regular surveys are used to identify early signs on trees, which are subsequently removed; control of the psyllid vector through survey and pesticide application; and replanting with clean plant material are all beneficial in places where HLB has not yet been established. Depending on the percentage of the canopy impacted, yield decline can range from 30% to 100% and is primarily caused by early abortion of fruits from afflicted branches ^[42].

2.3. Citrus Bacterial Disease

2.3.1. Citrus Canker Disease

Currently, citrus canker has been detected in over thirty countries, including Southeast Asia, South America, the islands of the Pacific and Indian Oceans. Due to its high susceptibility, among commercial citrus types and rootstocks, Asiatic citrus canker is particularly harmful to grapefruits (C. paradisi), limes (C. aurantifolia and C. limettioides), trifoliate oranges (Poncirus trifoliata), and their hybrids. Citrus fruits that are infected during the early stages of growth fracture or have malformations and the seriously infected fruits fall immaturely, even though only sporadic canker lesions may appear on the surface of fruits in later growth stages. Light infection renders fresh fruits unfit for commercial distribution. Fruit infections typically have a similar severity as foliage infections. In sensitive citrus trees that have already experienced severe foliage infection, fruit infection of 80% to 90% is not unusual. Such extreme defoliation, leaving only bare twigs, frequently results from such high foliage infection ^[43]. One of the biggest and most significant families of bacterial phytopathogens is the Xanthomonadaceae, which includes Xanthomonas citri subsp. citri. Citrus canker disease is caused by the pathogen X. citri subsp. citri, which has been extensively studied in terms of epidemiology and disease control as a pathogen of a worldwide significant fruit crop ^[44]. Conspicuous elevated necrotic lesions that form on leaves, twigs, and fruits identify infected plants as having them. By running the fingertips over the surface of affected tissues, lesions can be found. On leaves, they initially show as 2–10 mm round, oily-looking patches, typically on the abaxial surface (reflecting stomatal entry following rain dispersal). Lesions frequently have similar sizes. Later, tissue hyperplasia brought on by the infection may cause both epidermal surfaces to break. Circular lesions on leaves, stems, thorns, and fruits develop into elevated, blister-like lesions that eventually turn into white or yellow spongy pustules. These pustules eventually thicken and darken to become a corky, rough-to-the-touch canker that ranges in color from pale tan to brown. With transmitted light, it is simple to see the water-soaked border that frequently forms surrounding the necrotic tissue. Pustules on stems may group together to divide the epidermis throughout the length of the stem and, occasionally, immature stems may girdle. Older lesions on leaves and fruit typically have rising margins, a sunken center, and, occasionally, a yellow chlorotic halo around the edges (which may vanish as canker lesions age) ^[45]. The bacterium (Xanthomonas) is rod shaped, Gram negative, and has a single polar flagellum. It measures 1.5–2.0 × 0.5–0.75 mm. Growth requires aerobic activity. Because xanthomonadin pigment is produced, colonies on culture media are typically yellow. The use of resistant cultivars in combination with integrated systems of suitable cultural practices and phytosanitary measures, including quarantine and regulatory programs, results in the most successful management of canker. The fundamental tenets of the specific approaches include avoiding, excluding, or eradicating the pathogen, minimizing the spread of the pathogen, reducing the amount of inoculum available for infection, and protecting susceptible tissue against infection ^[46]. There have been reports of copper resistance in X. citri subsp. citri and X. alfalfae subsp. citrumelonis strains. The usage of copper-based bactericides, which are crucial substances for the management of Xanthomonas-related diseases on citrus, is seriously impacted by copper resistance ^[47].

2.3.2. Bacterial Blast Disease

More than 180 plant species, including Citrus spp., are infected by Pseudomonas syringae pv. syringae, which also produces black pits in orange fruits and bacterial blast in orange (C. sinensis) and mandarin (C. rediculate) fruits ^[48]^[49]. This disease has been reported in Iran, Montenegro, Tunisia, Turkey, and the USA ^[50]. Black spots on the petiole wings and water-soaked lesions were the first noticeable symptoms on leaves. Later lesions spread to the twigs surrounding the base of the petiole as well as to the midvein of the leaves. The leaves soon withered, rolled while remaining securely attached, and eventually fell to the ground without petioles. Twigs’ necrotic regions became larger and after 20 to 30 days, the twigs succumbed to death. A 50-hectare citrus plantation in Antalya suffered significant damage, with a disease prevalence of about 100%. The most popular therapy for a number of bacterial illnesses of fruit trees was the use of copper compound sprays (mostly the Bordeaux mixture) during the fall and winter before the infection P. syringae pv. syringae appears in late winter and spring ^[51]. The selection of copper-resistant P. syringae pv. syringae strains in mango orchards, where heavy copper spraying was utilized for disease management, may be the cause of their frequently reduced efficacy ^[52].

Table 1. Causes of losses and types of by-products during the production of citrus fruits.

Citrus Fruit Diseases		Types of by-Products	Citations
Citrus gumnosis	Pathogen: Phytophthora spp. Symptoms: Cankers and gum on citrus trunks and branches. The infection causes damage to fibrous roots in vulnerable rootstocks and crown rot, thereby causing fruit fall.	Roots, trunk, branches, shoots die off and fruit drop	^[31]^[32]^[33]
Citrus greening	Pathogen: Candidatus Liberibacter Symptoms: Pathogens infiltrate the phloem and assault the vascular system, blocking water and nutrient transport. Yellow shoots and mottled leaves with yellow midribs may occur causing die-back. Infected fruits are lobbed, have aborted seeds, and prematurely drop off.	Fruit drop	^[53]^[54]
Black rot	Pathogen: Alternaria spp. Symptoms: On fruits, symptoms range from light brown, depressed patches to dark brown circles. Young shoot apexes are defoliated in severely affected trees. Young infected fruits and leaves fall, and mature lesions-covered fruits are unmarketable. Alternaria spp. can cause black rot by causing latent infections on the calyx and disc, then entering the columella as the fruit grows.	Die shoots and fruit drops	^[55]^[56]^[57]
Brown rot	Pathogen: Phytophthora citrophthora and Phytophthora nicotianae Symptom: light brown, leathery decay. This disease is associated with citrus gummosis or citrus foot rot.	Fruit drops	^[58]^[59]^[60]^[61]
Anthracnose	Pathogen: Colletotrichum spp. Symptoms: The disease caused necrotic petals and fruit lesions during pre-harvesting. Infected twigs and lesions generally had black fructifications. During postharvest, the infected fruits had brown-to-black tear stains that turned silver-gray, 1.5 mm or bigger lesions.	Branch die-off, fruit drops during pre-harvesting stage and fruit loss during postharvesting	^[62]^[63]
Green and blue mold	Pathogen: Penicillium digitatum and P. italicum Symptoms: during postharvest, the fruit peel is soft and decolored and soaky. During disease development, the fruit surface is covered with aerial white mycelium turns to olive with spore development.	Fruit loss	^[64]^[65]
Sour rot	Pathogen: Geotrichum citri-aurantii Symptoms: Storage fruits in the humid condition cause the fungus growth with a light brown to yellow tint. The symptom appears extensive water-soaked lesions, and artroconidia and mycelia on the fruit surface.	Fruit loss	^[66]^[67]^[68]

3. Citrus Postharvest Disease

Filamentous fungi are the most common cause of citrus fruit postharvest diseases. Because of major changes in fruit features and environmental conditions, they are some of the most economically important pathogens that infect fruits in the field during the growing season and stay latent or quiescent until they resume growth after harvest. Alternaria sp. Ellis & N. Pierce in N. Pierce causes alternaria rot or black rot; Colletotrichum sp. (Penz.) Penz. & Sacc. in Penz. causes anthracnose; or Phytophthora spp. causes brown rot in Penz. Other economically significant diseases infect the fruits by rind wounds or damage sustained during harvest, transportation, or postharvest handling. Green and blue molds are caused by Penicillium digitatum (Pers.: Fr.) Sacc. and P. italicum Wehmer, respectively; sour rot is caused by Geotrichum citri-aurantii Ferraris E.E. Butler ^[69].

3.1. Black Rot Caused by Alternaria spp.

Alternaria spp. is responsible for a variety of citrus diseases, including alternaria brown spot in tangerines (Citrus reticulata Blanco) and black rot in a variety of Citrus spp. fruits ^[70]^[71]^[72]. The disease is a significant postharvest problem that may appear in the field prior to harvesting. In fruits, symptoms include light brown, slightly depressed spots to circular and dark brown areas on the external surface (Figure 1A). Young infected fruits and leaves frequently fall and mature fruits with lesions are unmarketable, resulting in significant economic losses ^[57]. During postharvest handling, extreme weather conditions, such as hot, dry summers and cool, moist winters, favor the disease. Citrus black rot begins as a core rot, in which the pathogen colonizes the fruit’s columella. The disease occurs most commonly on navel oranges and on tangerines and their hybrids during storage ^[73]. The fungus invades and colonizes the columella in black rot, which is usually a core rot. Except for the fact that the fruits are frequently more vividly colored than healthy fruit, there is usually little visible sign of infection. Infection can enter the fruits through wounds or natural apertures in the stylar end. The blossoms that have been affected by the fungus may wither before opening or drop off right after fruit set. Alternaria spp. can also cause black rot by forming latent infections on the calyx and disc, then invading the columella as the fruit matures ^[55]. Young leaves show irregular brown necrotic patches with characteristic yellow halos as symptoms ^[74]. In severely afflicted trees, the apex of young shoots is entirely defoliated. Citrus black rot disease can be caused by a variety of Alternaria species, including those that are not A. alternata citri ^[55].

Figure 1. Black rot of citrus fruit causes by Alternaria alternata, (A) = the symptom on fruit and leaf; (B) = colony and (C) = conidia morphology.

Morphologically, typical A. alternata colonies on potato dextrose agar media (PDA) are lettuce green to olive green in color, with a conspicuous (2–5 mm) white border and spread to a size larger than 70 mm in diameter after 7–10 days (Figure 1B). Based on the sporulation behaviors of single-spored colonies, A. alternata is distinguished by the formation of conidial chains six to fourteen conidia in length and the growth of several secondary, and rarely tertiary, chains, two to eight conidia in length. Through the extension of secondary conidiophores from distal terminal conidial cells and subsequent conidium production, chain branching happens in a sympodial way. Conidia are tiny (20.0–50.0 μm) length and oval in shape, with transverse and vertical walls dividing them and minimal apical extension growth (Figure 1C). The septate hyphae and conidiophores are light brown ^[56].

3.2. Brown Rot Caused by Phytophthora citrophthora

The fungi Phytophthora citrophthora (R. E. Sm. & E. H. Sm.) Leonian and P. nicotianae Breda de Haan (P. parasitica Dastur) are the most commonly connected with citrus foot rot, also known as gummosis or root rot ^[58]. It is commonly known as brown rot in storage fruits. Infected fruits when entering the packing house are frequently the major cause of postharvest deterioration issues in the entire batch. The infectious symptoms are leathery, light-brown lesions (Figure 2A) ^[61]. The morphological characteristics of Phytophthora spp. have been described ^[59]^[60]. Mycelium is thick and cotton like ^[75]. The colony is finely radiated with stellate and flame-like growth, growing at optimum temperatures of 24–28 °C (Figure 2B). Sporangiophores branch irregularly, with swelling at the point of branching. Some sporangia grow single or in loose sympodia, with a swelling at the branching point. Sporangia are noncaducous and generally papillate, with two apices that are often divergent. P. citrophthora makes sporangia in a variety of forms, including spherical, ovoid, obpyriform, obturbinate, and ellipsoid. Multiple papillae and offset pedicel attachments can cause distorted sporangial forms in water. Sporangia are 18.0–60.0 × 23.0–90.0 μm (average 30.0 × 45.0 μm). The length x breadth ratio is less than 1.6 (Figure 2C). Chlamydospores are rarely found on citrus isolates in culture, although they do form in the roots. Chlamydospores are 25.0–35.0 μm in diameter (average 28 μm). Hyphae are smooth and coarse and 3.0–7.0 μm in diameter ^[59]^[60].

Figure 2. Brown rot of citrus fruit causes by Phytophthora spp., (A) = the symptom on fruit; (B) = colony and (C) = morphology of sporangia.

3.3. Anthracnose Caused by Colletotrichum spp.

Colletotrichum spp. causes citrus anthracnose, which is a serious disease in many citrus-growing regions across the world. This disease has been reported in Algeria, Bermuda, Brazil, California, Italy, Mexico, Morocco, Pakistan, Portugal, Tunisia, and Turkey ^[63]^[76]^[77]^[78]^[79]. Many citrus species, including Mexican lime (C. aurantifolia), sweet orange (C. sinensis), and grapefruit (C. paradisi), have petal necrosis and necrotic lesions on their fruits. On mature fruits, brown to black streaks (tear stain) appeared, sometimes turning silver gray (Figure 3A). These lesions were 1.5 mm in diameter or greater. On the surface of the lesions and the dry extremities of diseased branches, dark-colored fructifications were found in general ^[62].

Figure 3. Black rot of citrus fruit causes by Colletotrichum gloeosporioides, (A) = the symptom on fruit; (B) = colony; and (C) = conidia morphology.

Morphologically, the mycelium in the colonies was creamy, white to pale gray, sparse, and more or less cottony, with profuse bright-orange conidiomata (acervuli) and setae (Figure 3B). Conidiophores within the conidiomata were branching with hyaline conidiogenous cells that were sub-cylindrical and more or less straight. Septate, brown, and slightly pale at the apex, setae were found (Figure 3C). Conidia (15.0 × 5.0 μm) mounted in lactic acid from actively growing colonies were hyaline and sub-cylindrical with bluntly rounded ends ^[62]^[63].

References

UN. Transforming Our World: The 2030 Agenda for Sustainable Development. Available online: https://sdgs.un.org/2030agenda (accessed on 17 May 2022).
Barros, M.V.; Salvador, R.; de Francisco, A.C.; Piekarski, C.M. Mapping of research lines on circular economy practices in agriculture: From waste to energy. Renew. Sustain. Energy Rev. 2020, 131, 109958.
Jacob-John, J.; D’Souza, C.; Marjoribanks, T.; Singaraju, S. Synergistic Interactions of SDGs in Food Supply Chains: A Review of Responsible Consumption and Production. Sustainability 2021, 13, 8809.
Madau, F.A.; Arru, B.; Furesi, R.; Pulina, P. Insect Farming for Feed and Food Production from a Circular Business Model Perspective. Sustainability 2020, 12, 5418.
Lim, M.K.; Lai, M.; Wang, C.; Lee, Y. Circular economy to ensure production operational sustainability: A green-lean approach. Sustain. Prod. Consum. 2022, 30, 130–144.
Esposito, B.; Sessa, M.R.; Sica, D.; Malandrino, O. Towards circular economy in the agri-food sector. A systematic literature review. Sustainability 2020, 12, 7401.
Zhang, Q.; Dhir, A.; Kaur, P. Circular economy and the food sector: A systematic literature review. Sustain. Prod. Consum. 2022, 32, 655–668.
Van Fan, Y.; Lee, C.T.; Lim, J.S.; Klemeš, J.J.; Le, P.T.K. Cross-disciplinary approaches towards smart, resilient and sustainable circular economy. J. Clean. Prod. 2019, 232, 1482–1491.
Sherwood, J. The significance of biomass in a circular economy. Bioresour. Technol. 2020, 300, 122755.
FAO. Citrus Fruit Fresh and Process; Food and Agriculture Organization of the United Nations: Rome, Italy, 2021.
El-Otmani, M.; Ait-Oubahou, A.; Zacarías, L. Citrus spp.: Orange, mandarin, tangerine, clementine, grapefruit, pomelo, lemon and lime. In Postharvest Biology and Technology of Tropical and Subtropical Fruits; Elsevier: Amsterdam, The Netherlands, 2011; pp. 437–516e.
Goldenberg, L.; Yaniv, Y.; Porat, R.; Carmi, N. Mandarin fruit quality: A review. J. Sci. Food Agric. 2018, 98, 18–26.
Forsyth, J.; Damiani, J. CITRUS FRUITS | Types on the Market. In Encyclopedia of Food Sciences and Nutrition, 2nd ed.; Caballero, B., Ed.; Academic Press: Oxford, UK, 2003; pp. 1329–1335.
Dutta, S.K.; Gurung, G.; Yadav, A.; Laha, R.; Mishra, V.K. Factors associated with citrus fruit abscission and management strategies developed so far: A review. N. Z. J. Crop Hortic. Sci. 2022, 1–22.
Gulfishan, M.; Jahan, A.; Bhat, T.A.; Sahab, D. Chapter 16-Plant Senescence and Organ Abscission. In Senescence Signalling and Control in Plants; Sarwat, M., Tuteja, N., Eds.; Academic Press: Cambridge, MA, USA, 2019; pp. 255–272.
Sawicki, M.; Aït Barka, E.; Clément, C.; Vaillant-Gaveau, N.; Jacquard, C. Cross-talk between environmental stresses and plant metabolism during reproductive organ abscission. J. Exp. Bot. 2015, 66, 1707–1719.
Iglesias, D.J.; Cercós, M.; Colmenero-Flores, J.M.; Naranjo, M.A.; Ríos, G.; Carrera, E.; Ruiz-Rivero, O.; Lliso, I.; Morillon, R.; Tadeo, F.R. Physiology of citrus fruiting. Braz. J. Plant Physiol. 2007, 19, 333–362.
Gustafsson, J.; Cederberg, C.; Sonesson, U.; Emanuelsson, A. The Methodology of the FAO Study: Global Food Losses and Food Waste-Extent, Causes and Prevention-FAO, 2011; SIK Institutet för Livsmedel och Bioteknik: Borås, Sweden, 2013.
Perondi, D.; Fraisse, C.W.; Dewdney, M.M.; Cerbaro, V.A.; Andreis, J.H.D.; Gama, A.B.; Junior, G.J.S.; Amorim, L.; Pavan, W.; Peres, N.A. Citrus advisory system: A web-based postbloom fruit drop disease alert system. Comput. Electron. Agric. 2020, 178, 105781.
Lima, W.G.; Spósito, M.B.; Amorim, L.; Gonçalves, F.P.; de Filho, P.A.M. Colletotrichum gloeosporioides, a new causal agent of citrus post-bloom fruit drop. Eur. J. Plant Pathol. 2011, 131, 157.
Huchche, A.; Ladaniya, M. Citrus Flowering and Fruiting—Recent Research Advances. In Proceedings of the Souvenir, National Seminar-Cum-Workshop on Physiology of Flowering in Perennial Fruit Crops; Central Institute for Subtropical Horticulture (ICAR): Lucknow, India, 2014; pp. 74–88.
Syvertsen, J.; Garcia-Sanchez, F. Multiple abiotic stresses occurring with salinity stress in citrus. Environ. Exp. Bot. 2014, 103, 128–137.
Sato, K. Influence of drought and high temperature on citrus. In Abiotic Stress Biology in Horticultural Plants; Springer: Berlin/Heidelberg, Germany, 2015; pp. 77–86.
Urbaneja, A.; Grout, T.G.; Gravena, S.; Wu, F.; Cen, Y.; Stansly, P.A. Chapter 16-Citrus pests in a global world. In The Genus Citrus; Talon, M., Caruso, M., Gmitter, F.G., Eds.; Woodhead Publishing: Cambridge, UK, 2020; pp. 333–348.
Khamsaw, P.; Lumsangkul, C.; Karunarathna, A.; Onsa, N.E.; Kawichai, S.; Chuttong, B.; Sommano, S.R. Recovery of Orange Peel Essential Oil from ‘Sai-Namphaung’ Tangerine Fruit Drop Biomass and Its Potential Use as Citrus Fruit Postharvest Diseases Control. Agriculture 2022, 12, 701.
Moraes Bazioli, J.; Belinato, J.R.; Costa, J.H.; Akiyama, D.Y.; Pontes, J.G.d.M.; Kupper, K.C.; Augusto, F.; de Carvalho, J.E.; Fill, T.P. Biological control of citrus postharvest phytopathogens. Toxins 2019, 11, 460.
Talibi, I.; Boubaker, H.; Boudyach, E.; Ait Ben Aoumar, A. Alternative methods for the control of postharvest citrus diseases. J. Appl. Microbiol. 2014, 117, 1–17.
Graham, J.; Feichtenberger, E. Citrus Phytophthora diseases: Management challenges and successes. J. Citrus Pathol. 2015, 2.
Singh, K.; Sharma, R.; Dubey, A.; Kamil, D.; Lekshmy, S.; Awasthi, O.; Jha, G. Phytophthora Nicotianae Breda de Haan Induced Stress Changes in Citrus Rootstock Genotypes; NISCAIR-CSIR: New Delhi, India, 2019.
Rajput, N.A.; Atiq, M.; Tariq, H.; Saddique, W.M.; Hameed, A. Citrus Gummosis: A Formidable challenge to citrus industry: A Review. Int. J. Biosci. 2020, 16, 131–144.
Gottwald, J.R.; Krysan, P.J.; Young, J.C.; Evert, R.F.; Sussman, M.R. Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proc. Natl. Acad. Sci. USA 2000, 97, 13979–13984.
Erwin, D.C.; Ribeiro, O.K. Phytophthora: Diseases Worldwide; APS Press: St. Paul, MN, USA, 1996.
Timmer, L.W.; Duncan, L.W. Citrus Health Management; APS Press: St. Paul, MN, USA, 1999.
Savita, G.S.V.; Nagpal, A. Citrus diseases caused by Phytophthora species. GERF Bull. Biosci. 2012, 3, 18–27.
Agrios, G.N. Plant Pathology; Elsevier: Amsterdam, The Netherlands, 2005.
Lee, R.F. Chapter Five-Control of Virus Diseases of Citrus. In Advances in Virus Research; Loebenstein, G., Katis, N.I., Eds.; Academic Press: Cambridge, MA, USA, 2015; Volume 91, pp. 143–173.
Berk, Z. Chapter 5-Diseases and pests. In Citrus Fruit Processing; Berk, Z., Ed.; Academic Press: San Diego, CA, USA, 2016; pp. 83–93.
Methacanon, P.; Krongsin, J.; Gamonpilas, C. Pomelo (Citrus maxima) pectin: Effects of extraction parameters and its properties. Food Hydrocoll. 2014, 35, 383–391.
Plaza, P.; Torres, R.; Usall, J.; Lamarca, N.; Vinas, I. Evaluation of the potential of commercial post-harvest application of essential oils to control citrus decay. J. Hortic. Sci. Biotechnol. 2004, 79, 935–940.
Gasparoto, M.; Coletta-Filho, H.; Bassanezi, R.; Lopes, S.; Lourenço, S.; Amorim, L. Influence of temperature on infection and establishment of ‘Candidatus Liberibacter americanus’ and ‘Candidatus Liberibacter asiaticus’ in citrus plants. Plant Pathol. 2012, 61, 658–664.
Dala-Paula, B.M.; Plotto, A.; Bai, J.; Manthey, J.A.; Baldwin, E.A.; Ferrarezi, R.S.; Gloria, M.B.A. Effect of Huanglongbing or Greening Disease on Orange Juice Quality, a Review. Front. Plant Sci. 2019, 9, 1976.
Gottwald, T.R. Current Epidemiological Understanding of Citrus Huanglongbing. Annu. Rev. Phytopathol. 2010, 48, 119–139.
Goto, M. Citrus canker. In Plant Diseases of International Importance. Vol. III. Diseases of Fruit Crops; Kumar, J., Chaube, H.S., Singh, U.S., Mukhopadhyay, A.N., Eds.; Prentice Hall: Englewood Cliffs, NJ, USA, 1992; pp. 170–208.
Ference, C.M.; Gochez, A.M.; Behlau, F.; Wang, N.; Graham, J.H.; Jones, J.B. Recent advances in the understanding of Xanthomonas citri ssp. citri pathogenesis and citrus canker disease management. Mol. Plant Pathol. 2018, 19, 1302.
Das, A. Citrus canker-A review. J. Appl. Hortic. 2003, 5, 52–60.
Civerolo, E. Citrus bacterial canker disease: An overview. In Proceedings of the International Society of Citriculture, Okitsu, Japan, 9–12 November 1981; pp. 390–394.
Behlau, F.; Gochez, A.M.; Jones, J.B. Diversity and copper resistance of Xanthomonas affecting citrus. Trop. Plant Pathol. 2020, 45, 200–212.
Smith, C.O.; Fawcett, H.S. A comparative study of the Citrus blast bacterium and some other allied organisms. J. Agric. Res. 1930, 41, 233–246.
Mirik, M.; Baloglu, S.; Aysan, Y.; Cetinkaya-Yildiz, R.; Kusek, M.; Sahin, F. First outbreak and occurrence of citrus blast disease, caused by Pseudomonas syringae pv. syringae, on orange and mandarin trees in Turkey. Plant Pathol. 2005, 54, 238.
Abdellatif, E.; Kałużna, M.; Ferrante, P.; Scortichini, M.; Bahri, B.; Janse, J.D.; van Vaerenberg, J.; Baeyen, S.; Sobiczewski, P.; Rhouma, A. Phylogenetic, genetic, and phenotypic diversity of Pseudomonas syringae pv. syringae strains isolated from citrus blast and black pit in Tunisia. Plant Pathol. 2020, 69, 1414–1425.
Mougou, I. Citrus Blast and Black Pit Disease: A Review. DYSONA-Life Sci. 2022, 3, 1–6.
Cazorla, F.M.; Arrebola, E.; Olea, F.; Velasco, L.; Hermoso, J.M.; Pérez-García, A.; Tores, J.A.; Farre, J.M.; de Vicente, A. Field evaluation of treatments for the control of the bacterial apical necrosis of mango (Mangifera indica) caused by Pseudomonas syringae pv. syringae. Eur. J. Plant Pathol. 2006, 116, 279–288.
Berk, Z. Citrus Fruit Processing; Academic Press: Cambridge, MA, USA, 2016.
Lee, R.F. Control of virus diseases of citrus. Adv. Virus Res. 2015, 91, 143–173.
Brown, G.; McCornack, A. Decay caused by Alternaria citri in Florida citrus fruit. Plant Dis. Report. 1972, 909–912.
Troncoso-Rojas, R.; Tiznado-Hernández, M.E. Alternaria alternata (black rot, black spot). In Postharvest Decay; Elsevier: Amsterdam, The Netherlands, 2014; pp. 147–187.
Vicent, A.; Armengol, J.; Sales, R.; García-Jiménez, J.; Alfaro-Lassala, F. First report of Alternaria brown spot of citrus in Spain. Plant Dis. 2000, 84, 1044.
Fagoaga, C.; Rodrigo, I.; Conejero, V.; Hinarejos, C.; Tuset, J.J.; Arnau, J.; Pina, J.A.; Navarro, L.; Peña, L. Increased tolerance to Phytophthora citrophthora in transgenic orange plants constitutively expressing a tomato pathogenesis related protein PR-5. Mol. Breed. 2001, 7, 175–185.
Bawage, S.; Nerkar, S.; Kumar, A.; Das, A. Morphological and molecular description of Phytophthora insolita isolated from citrus orchard in India. J. Mycol. 2013, 2013, 247951.
Das, A.; Nerkar, S.; Kumar, A.; Bawage, S. Detection, identification and characterization of Phytophthora spp. Infecting citrus in India. J. Plant Pathol. 2016, 98, 55–69.
Smith, R.E.; Smith, E.H. A new fungus of economic importance. Bot. Gaz. 1906, 42, 215–221.
Rhaiem, A.; Taylor, P.W. Colletotrichum gloeosporioides associated with anthracnose symptoms on citrus, a new report for Tunisia. Eur. J. Plant Pathol. 2016, 146, 219–224.
Pérez-Mora, J.L.; Mora-Romero, G.A.; Beltrán-Peña, H.; García-León, E.; Lima, N.B.; Camacho-Tapia, M.; Tovar-Pedraza, J.M. First Report of Colletotrichum siamense and C. gloeosporioides Causing Anthracnose of Citrus spp. in Mexico. Plant Dis. 2021, 105, 496.
Palou, L. Penicillium digitatum, Penicillium italicum (green mold, blue mold). In Postharvest Decay; Elsevier: Amsterdam, The Netherlands, 2014; pp. 45–102.
Papoutsis, K.; Mathioudakis, M.M.; Hasperué, J.H.; Ziogas, V. Non-chemical treatments for preventing the postharvest fungal rotting of citrus caused by Penicillium digitatum (green mold) and Penicillium italicum (blue mold). Trends Food Sci. Technol. 2019, 86, 479–491.
Suprapta, D.N.; Arai, K.; Iwai, H. Distribution of Geotrichum candidum citrus race in citrus groves and non-citrus fields in Japan. Mycoscience 1995, 36, 277–282.
McKay, A.H. Population Structure of the Sour Rot Pathogens Galactomyces citri-aurantii and G. geotrichum and Evaluation of Sterol Demethylation Inhibitors for Postharvest Management of Citrus Decays; University of California: Riverside, CA, USA, 2011.
Nazerian, E.; Alian, Y.M. Association of Geotrichum citri-aurantii with citrus fruits decay in Iran. Int. J. Agron. Plant Prod. 2013, 4, 1839–1843.
Palou, L. Control of citrus postharvest diseases by physical means. Tree For. Sci. Biotechnol. 2009, 3, 127–142.
Timmer, L.W.; Akimitsu, K.; Solel, Z.; Peever, T. Alternaria diseases of citrus-novel pathosystems. Alternaria Dis. Citrus-Nov. Pathosyst. 2003, 42, 99–112.
Carvalho, D.D.; Alves, E.; Batista, T.R.; Camargos, R.B.; Lopes, E.A. Comparison of methodologies for conidia production by Alternaria alternata from citrus. Braz. J. Microbiol. 2008, 39, 792–798.
Aiello, D.; Guarnaccia, V.; Azzaro, A.; Polizzi, G. Alternaria brown spot on new clones of sweet orange and lemon in Italy. Phytopathol. Mediterr. 2020, 59, 131–145.
Varano, A.; Shirahigue, L.D.; Azevedo, F.A.; Altenhofen da Silva, M.; Ceccato-Antonini, S.R. Mandarin essential oil as an antimicrobial in ethanolic fermentation: Effects on Limosilactobacillus fermentum and Saccharomyces cerevisiae. Lett. Appl. Microbiol. 2022, 74, 981–991.
Sommano, S.; Joyce, D.; Dinh, S.; D’arcy, B. Infection by Alternaria alternata causes discolouration of Backhousia myrtifolia foliage and flowers. J. Hortic. Sci. Biotechnol. 2012, 87, 41–46.
Martin, F.N.; Abad, Z.G.; Balci, Y.; Ivors, K. Identification and detection of Phytophthora: Reviewing our progress, identifying our needs. Plant Dis. 2012, 96, 1080–1103.
Vitale, A.; Aiello, D.; Azzaro, A.; Guarnaccia, V.; Polizzi, G. An eleven-year survey on field disease susceptibility of citrus accessions to Colletotrichum and Alternaria species. Agriculture 2021, 11, 536.
Wang, W.; de Silva, D.D.; Moslemi, A.; Edwards, J.; Ades, P.K.; Crous, P.W.; Taylor, P.W. Colletotrichum species causing anthracnose of citrus in Australia. J. Fungi 2021, 7, 47.
Riolo, M.; Aloi, F.; Pane, A.; Cara, M.; Cacciola, S.O. Twig and shoot dieback of citrus, a new disease caused by Colletotrichum species. Cells 2021, 10, 449.
Uysal, A.; Kurt, Ş.; Guarnaccia, V. Distribution and characterization of Colletotrichum species associated with Citrus anthracnose in eastern Mediterranean region of Turkey. Eur. J. Plant Pathol. 2022, 163, 125–141.

© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.

Upload a video for this entry

Information

Subjects: Horticulture

Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :

Pattarapol Khamsaw

Jiraporn Sangta

Pirawan Chaiwan

Pornchai Rachtanapun

Sasithorn Sirilun

Korawan Sringarm

Sarinthip Thanakkasaranee

Sarana Rose Sommano

View Times: 1.2K

Update Date: 31 Aug 2022

Table of Contents

Video Upload Options

Confirm