Introduction

Sharka, also known as ‘Plum pox’, is by far the most harmful viral disease of stone fruits worldwide. It is caused by plum pox virus (PPV), a potyvirus in the Potyviridae family, which infects major stone fruit trees of the genus Prunus (Rosaceae family), including apricot (P. armeniaca), peach (P. persica), plum (P. domestica) and cherry (P. avium; García et al., 2014; Sheveleva et al., 2018), as well as other ornamental and wild Prunus species (James & Thompson, 2006; Sebestyen et al., 2008). PPV spread at local scale is mainly caused by aphids (e.g., Myzus persicae, Phorodon humuli and Hyalopterus pruni; Isac et al, 1998), and common herbaceous species (e.g., Bellis perennis, Clematis sp., Convolvulus arvensis, Matricaria chamomilla, Taraxacum officinalis, and Trifolium sp.) may represent important secondary sources of this disease in orchards (Llácer, 2006; Manachini et al., 2007; Moreno et al., 2009). Differently, the long-distance diffusion of PPV has been due to global trade of infected plant material (García et al., 2014).

Identified for the first time in 1918 in Bulgaria (Atanasoff, 1932), PPV is currently widespread in Europe, the Middle East, North and South America, and Asia (EPPO, 2022). The worldwide PPV genetic characterization identified ten strains (Chirkov et al., 2018; James et al., 2013): PPV-Marcus (M), PPV-Dideron (D), PPV-Recombinant (Rec), PPV-El Amar (EA), PPV-Cherry (C), PPV-Winona (W), PPV-Turkey (T), PPV-Cherry Russian (CR), PPV-Ancestor (An), and the recent PPV-Cherry Volga (CV). PPV-M, PPV-D and PPV-Rec have been most widely reported, with PPV-M as the most aggressive virus which is efficiently transmitted by aphids, whereas PPV-D being the most widely distributed, and PPV-Rec (efficiently transmitted by aphids as well) being the recombinant product of PPV-M with PPV-D (García et al, 2014; Sihelská et al., 2017).

Symptoms of sharka may appear on leaves, shoots, barks, petals, fruits and stones (apricot and only a few sensitive plum cultivars; Fig. 1). They are clearly visible on leaves early in the growing season and include mild light-green discoloration, chlorotic spots, bands or rings, vein clearing or yellowing and leaf deformation. Flower symptoms can occur on petals (discoloration), especially in peach cultivars with pink flowers. Infected fruits show chlorotic spots or lightly pigmented yellow rings or line patterns (especially in Japanese plums and peaches). They may become deformed or show irregular shape (especially cherries and plums), and over time may develop brown or necrotic areas under the discolored rings. Furthermore, premature fruit drop was observed in apricot, European plum, sweet and sour cherry. Fruits of early maturing cultivars of all susceptible species usually show more severe symptoms than those of late maturing ones (Revers & García, 2015; Sochor et al., 2012). Thus, although sharka poses no danger to consumers, it can make stone fruits unmarketable.

Fig. 1
figure 1

Symptoms induced by plum pox virus on (i) apricot leaves (A), fruits (B) and stone (C); (ii) peach leaves (D), fruits (E) and petals (F); and (iii) plum leaves (G) and fruit (H); and premature plum fruit drop (I; EPPO, 2023)

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As infected trees cannot be treated, but only removed and destroyed, the management of the disease is possible only by prevention, using PPV-free propagation material, contrast to PPV vectors, and field monitoring for PPV presence (García et al., 2014; Labonne & Dallot, 2006; Llácer, 2006). Actually, visual symptoms are not always a reliable indicator of disease as they can occur after several months or years after the tree has been infected, and other viruses can enhance the symptoms (e.g., pseudosharka; Wilhelm & Kunze, 1995). Thus, PPV can be more reliably detected by laboratory analysis of tissue samples or by grafting test material onto highly susceptible hosts and monitoring for the development of symptoms. The impact of sharka disease over 30 years was thus estimated to be over 10,000 million euros, taking into account the economic losses in production and the costs of sanitary control and surveillance, and of eradication programmes run in affected countries worldwide (Cambra et al., 2006a; Rubio et al., 2017).

For these reasons, PPV was ranked as quarantine pest in European Union since 2000 (European Council, 2000), although in 2019 it was regraded to ‘regulated non-quarantine pest’ (RNQP) due to its widespread endemic presence (European Union, 2019). However, the attention paid to PPV challenging stone fruits is still tremendous, as demonstrated by the number of studies and reviews focused on this topic (De Mori et al., 2020; Espinoza et al., 2021; Gürcan et al., 2021; Kil et al., 2021; Maejima et al., 2020; Mori et al., 2021; Okić et al., 2022; Rodamilans et al, 2020; Tamukong et al., 2020).

Europe is a major producer of stone fruits with around 8 million tons produced annually, mostly peaches, plums, cherries and apricots, and Italy is the most ardent contributor, together with Spain. Stone fruit production is of economic importance in Italy, especially of the cultivation of peaches, apricots, plums and cherries (around 1 million, 200,000, 140,000 and 90,000 tons produced in 2021, respectively; FAOSTAT, 2021). However, Italian stone fruit production (as well as other analogous markets worldwide) is continually challenged by sharka, which was firstly identified in Italy in the 1970s (Alber et al., 1974), and has been reported in most Italian regions (Armentano & Bertanza, 2018; Bianco et al., 2005). In Italy, the first regulation about sharka control was established in 1996, and it was based on field monitoring, eradication of infected plants, obligation to use certified propagation material in new orchards, multiplication of only healthy plant material, and destruction of infected mother plants in the nursery (Italian Republic, 1996). In accordance with the European regulation, a new decree was adopted in 2009, which introduced a subdivision among settlement (i.e., infected area where the disease was no longer eradicable), outbreak (i.e., infected area where diseased plants had to be removed, and plants could not be recovered for multiplication), buffer (i.e., not infected area, but close to outbreak and/or settlement zones) and free zones (i.e., not infected area; Italian Republic, 2009). Due to the impossibility of PPV eradication in several Italian areas, some deregulations occurred in 2016 (e.g., reduction of the buffer zone radius from 1 km to 300 m around an infected plant; Italian Republic, 2016) and the decree was finally abrogated in 2021 (Italian Republic, 2021), following the abovementioned PPV downregulation to RNQP by the European Union.

Although several studies and monitoring activities of sharka and its causal agent PPV have been carried out in the last decades, information on the diffusion of the disease in Italy is still scattered and incomplete (e.g., data from specific regions are missing or unavailable). To address this knowledge gap, the present review aimed to firstly provide a historical overview of sharka in Italy, summarizing outcomes on the disease and its causal agent PPV occurred around fifty years ago, also with a further focus on Tuscany (Central Italy). We anticipate that outcomes here reported will be useful for the understanding of genetic diversity and diffusion of sharka in Italy, thus encouraging other research in this area and supporting the challenging contrast to this detrimental disease.

Data recovery

A database reporting peer-reviewed and official information about the diffusion of sharka and its causal agent PPV in Italy was created on May 2023 examining (i) published peer-reviewed literature, (ii) regional laws concerning sharka, reports of sharka monitoring activities and/or informative materials published in websites of regional phytosanitary services (RPS) and other institutions (26 online resources and databases were used, list provided in Supplementary Table S1), and (iii) personal communications obtained from reliable institutions (Table S1).

The published peer-reviewed literature was searched in the Web of Science (Thompson-ISI, Philadelphia, PA, USA), Scopus (Elsevier, Amsterdam, Netherlands), Science Direct (Elsevier) and Google Scholar (Google, Mountain View, CA USA) databases (see websites in Table S1), using multiple combinations of “sharka”, “vaiolatura delle drupacee” (i.e., the common Italian name of sharka), “Plum pox virus”, “PPV”, “PPV-M”, “PPV-Rec”, “PPV-D”, “Prunus”, “peach”, “apricot”, plum” and “Italy” as keywords. Several peer-reviewed papers were dated and not available in digital format, so they were retrieved by the library service of the Department of Agriculture, Food and Environment of the University of Pisa (using also intra-university book lending). The reference lists of any article identified by this literature search were cross-checked in order to include any other relevant reference, finally identifying 28 research papers (Table 1). These articles were used together with 45 official documents and 15 personal communications (Supplementary Table S1).

Table 1 Year, region, host and strain [PPV-Dideron (D), PPV-Marcus (M), PPV-Recombinant (Rec)] of plum pox virus identifications reported in published research papers (n = 28). na: not available; *: for Trentino-Alto Adige region, Bolzano or Trento autonomous provinces are specified
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Recovered data were screened to get the following information for each Italian region: (i) year of the first identification of sharka, (ii) number of districts affected by sharka, (iii) PPV strains reported by enzyme-linked immunosorbent assay (ELISA) or polymerase chain reaction (PCR) methods, and (iv) Prunus hosts of PPV. Furthermore, given the long-lasting collaboration between the Department of Agriculture, Food and Environment (DAFE) of the University of Pisa (i.e., Author institution) and the Regional Phytosanitary Service of Tuscany (RPS-T) more information was recovered for this Region, namely (i) the sites investigated during the PPV monitoring campaigns, (ii) the samples positive to PPV, and (iii) the identified PPV strains.

Sharka in Italy

Sharka spread across almost the whole Italian peninsula, and the regions with higher rates of infected districts are not always those more dedicated to the production of stone fruits

The history of sharka in Italy began about 50 years ago (i.e., 1970s) in north-eastern regions, with the identifications by Alber et al. (1974) in Alto Adige and a few years later by Canova et al. (1977) in nearby Trentino (Fig. 2a). In the 1980s, the disease was then randomly recovered in other northern regions (Emilia-Romagna and Piedmont; Conti et al., 1984; Giunchedi et al., 1983), and later also in central (Lazio; Barba et al., 1985) and southern regions (Apulia, Basilicata and Sicily; Davino et al., 1986; Di Terlizzi et al., 1988). Similarly, in the 1990s, sharka was firstly reported in a further six regions erratically scattered along the country as (following a chronologic order) it was identified in Calabria (Southern Italy; Polizzi & Agosteo, 1992), Abruzzo (Central Italy; Vicchi & Babini, 2008), Tuscany (Central Italy; Ginanni et al., 1993), Friuli-Venezia Giulia (Northern Italy; Pasquini & Barba, 1994), Lombardy (Northern Italy; Vicchi & Babini, 2008), Veneto (Northern Italy; Poggi Pollini et al., 1996) and Campania (Southern Italy; Carella et al., 2002). At the beginning of the new millennium, sharka was also reported in the Marche region (Central Italy; Marche Region, 2018), whereas the most recent first report was by Palmisano et al. (2011) in Molise (Central Italy). The presence of sharka was confirmed also in Sardinia, but no data were retrieved about the year of introduction (Sardinia Region, 2016). Thus, sharka has never been reported in Liguria, Umbria and Aosta Valley (Personal communications), probably due to the scarcity of stone fruit orchards in these regions (ISTAT, 2021). Overall, these outcomes clearly show that sharka spread across almost the whole Italian peninsula from its first identification around 50 years ago, but its scattered diffusion (as well as its presence reported in island regions) suggests that its dissemination occurred not only because of aphid transmission but more importantly by accidental movement of infected plant material.

Fig. 2
figure 2

(A) Year of the first identification of sharka, and (B) number of districts with farms affected by sharka for each Italian region. N.P. = not present; ? = sharka was reported, but no data were retrieved about the year of identification

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All districts of Emilia-Romagna (i.e., the region with the second higher production of stone fruits: about 200,000 tons produced annually vs about 71,000 tons as average among Italian regions; ISTAT, 2021) and the Trentino-Alto Adige regions were affected by sharka, as well as 60% of the districts of Campania (i.e., the region with the highest production of stone fruits: about 511,000 tons; ISTAT, 2021). The disease was observed in half of the districts of the Basilicata (i.e., the region with the fourth higher production of stone fruits: 110,000 tons; ISTAT, 2021), Friuli-Venezia Giulia, Apulia and Molise. Lower rates of sharka presence were reported for the other regions, including Sicily (i.e., the region with the third higher production of stone fruits: 140,000 tons; ISTAT, 2021; Fig. 2b). These data indicate that the regions with a larger fraction of infected districts are not always those more dedicated to the production of stone fruits. Evidently, a reliable interpretation of these results has to consider also the extension, district numbers and the production of each region. For example, comparing Campania and Trentino-Alto Adige which have approximately the same territorial area (around 13,600 km2), Campania showed a small fraction of affected districts compared to Trentino-Alto Adige (60 vs 100%). The impact of sharka is larger in Campania being the major stone fruit producer in Italy, while the production in Trentino-Alto Adige is lower (about 4,300 tons produced annually; ISTAT, 2021) as this region is more dedicated to other fruits (i.e., apples, pears and grapevine).

Major PPV strains, i.e., PPV-D, PPV-M and PPV-Rec, have been reported in apricot, peach and plum

Only the three major PPV strains causing sharka, i.e., PPV-D, PPV-M and PPV-Rec, have been reported in Italy (actually, the PPV-C strain was identified once in Apulia in a single sweet cherry tree which was immediately eradicated, and PPV-C was never found again; Crescenzi et al., 1994). The occurrence of the PPV-D, PPV-M and PPV-Rec strains is in accordance with other European regions (Cambra et al., 2006b; Kamenova & Borisova, 2019; Vidal et al., 2020; Zagrai et al., 2009; Fig. 3a). Taking into account the observed presence of these strains, Italian regions could be divided into four groups: (i) Calabria and Lazio with only PPV-D reported, (ii) Abruzzo and Molise with only PPV-M, (iii) Basilicata, Friuli-Venezia-Giulia, Lombardy, Marche, Piedmont, Sicily, Trentino-Alto Adige and Veneto with both PPV-D and PPV-M, and (iv) Campania, Emilia-Romagna, Tuscany and Apulia where all the three strains PPV-D, PPV-M and PPV-Rec have been reported. Thus, PPV-M and PPV-D were the most reported (mostly together) with 14 regions involved, whereas PPV-Rec was observed only in four regions. Actually, the low presence of PPV-Rec could be due to a misidentification of this strain with PPV-M because PPV-Rec was recognized only in 2004 as product of a recombinant event between PPV-D and PPV-M (Glasa et al., 2004). Moreover, the coat proteins targeted by several diagnostic methods are similar for the PPV-M and PPV Rec strains often leading to a wrong diagnosis, especially in the past (James et al., 2013).

Fig. 3
figure 3

(A) Plum pox virus (PPV) strains, and (B) Prunus hosts of PPV (apricot, peach and plum) reported in each Italian region

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PPV was reported only in apricot, peach and plum (other than the single identification in sweet cherry reported above; Crescenzi et al., 1994). All three species were reported as PPV hosts in most of the regions (Fig. 3b), except for Calabria (only apricot), Molise and Sardinia (only peach), Abruzzo and Sicily (only apricot and peach), and Apulia and Lazio (only apricot and plum). Thus, all three species were reported as PPV hosts mostly in northern regions, whereas a larger hostspecificity was observed in central and southern ones. Overall, these outcomes were expected as apricot, peach and plum are widespread and economically relevant species, and for these reasons have been monitored intensively (Umer et al., 2019). However, it is important to highlight that other minor commercial (e.g., almond), ornamental (e.g., cherry laurel) and spontaneous (e.g., blackthorn) Prunus species (García et al., 2014) reported as PPV hosts (and inoculum sources) have not been investigated so far, and further research should be conducted to elucidate their role in the diffusion of sharka in Italy.

A focus on Tuscany

Sharka has been reported in Tuscany since the 1990s, and extensive PPV monitoring campaigns were run from 2013 to 2021, especially in nurseries

Tuscany is one of the major regions of Central Italy in terms of stone fruit production (ISTAT, 2021). As reported above, sharka was here firstly identified in the early 1990s on apricot and plum (Ginanni et al., 1993), but it became a serious threat only with a new outbreak in 2013, when RPS-T reported the disease on plums growing in commercial orchards and a nursery (Tuscany Region, 2013). As a consequence, according to the national legislation (Italian Republic, 2009), a specific Tuscany regional decree aimed to implement sharka monitoring and management methods was established in 2014 (Tuscany Region, 2014) and updated in 2019 (Tuscany Region, 2019), although it was abrogated in 2021 with the Italian reception of EU regulation which downregulated PPV to RNQP (Italian Republic, 2021).

From 2013 to 2021, RPS-T (in collaboration with DAFE) performed sharka monitoring, extensively surveying a total of 1,596 sites characterized by the presence of commercial apricots, peaches, plums, sweet cherries, ornamental myrabolan plums and wild blackthorns. Nurseries were mostly inspected (n = 1217), followed by farms (n = 327) and non-agricultural areas (n = 52; Fig. 4a). The number of surveyed sites increased every year due to the increasing number of monitored nurseries. The number of farms and non-agricultural sites did not change much. Actually, Tuscany is characterized by an ancient nursery tradition, with this business being not only an Italian, but also a European excellence, at both quantitative and qualitative levels, especially for ornamental plants (Lazzerini et al., 2016). This feature, together with the fact that nurseries can play a key role in the spread of plant diseases, being departure and arrival hubs of plant material marketed all around the world (Alonso Chavez et al., 2016; Pisuttu et al., 2023), explains why PPV monitoring was mostly focused in nurseries. During these RPS-T/DAFE surveys, sharka-like symptoms were observed on a total of 5,240 plants (which were collected for diagnostic analyses), among which 3,070, 1,740, and 430 samples were recovered in farms, nurseries and non-agricultural areas, respectively. Peaks in collected samples (n = ca. 700–800) occurred in 2016, 2017, and 2020, whereas lowest amount was sampled in 2013 (n < 200), so showing an irregular trend over the years (Fig. 4b).

Fig. 4
figure 4

(A) Number (n) of sites and (B) samples collected in farms, nurseries and non-agricultural areas of Tuscany during the 2013–2021 sharka monitoring campaigns

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Higher number of symptomatic and PPV positive samples were recorded in farms, mostly in Arezzo and Florence districts, and only PPV-M and PPV-Rec strains seem still present in Tuscany

Overall, around 4% of the collected samples tested positive for sharka, with higher numbers of infected samples reported in 2014 and 2018 (n = 41 and 37, respectively), and lowest in 2017 (n = 7), thus not showing a clear trend over the years (Fig. 5). As expected, most of the positive samples were collected in farms (n = 211), as only six and two positive samples were from nurseries and non-agricultural areas, respectively, thus showing no relation between the number of collected samples and those testing positive (this feature being true also taking into account the years of monitoring). The larger number of positive samples in farms was likely due to more favourable conditions for the spread of the disease (e.g., vectors, environmental conditions) and less survey activities, compared to nurseries (although the large number of potential hosts).

Fig. 5
figure 5

Number (n) of plum pox virus positive samples for each type of site (farms, non-agricultural areas, nurseries) during the 2013–2021 sharka monitoring campaigns run in Tuscany

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Sharka was reported only in six Tuscan districts, mostly and continuously in Arezzo and Florence, whereas more discontinuously in Grosseto and Pistoia, and only once in Lucca and Siena (Fig. 6). Other than the four districts reported above for identifications in farms (Fig. 2b), identifications in nurseries occurred in Pistoia and Siena districts, where no positive samples were reported in other area types. These outcomes showed that most affected districts were those with a higher density of stone fruit farms (ISTAT, 2021).

Fig. 6
figure 6

Districts where sharka was reported during the 2013–2021 sharka monitoring campaigns run in Tuscany (gray). The years of sharka detection in farms (F), non-agricultural areas (NAA) and nurseries (N) are reported

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Although only PPV-D strain was reported in the whole Italy until 1996 (Poggi Pollini et al., 1996), a genetic characterization of PPV strains isolated from stone fruits (apricot, peach, plum) of Tuscany collected in 2020 and 2021 allowed to identify also PPV-M, mostly in peach and less in plum, whereas PPV-Rec was identified only in plum (Pedrelli et al., 2023). This divergence among PPV strain/host relations was already reported (Sihelská et al., 2017), and the lack of PPV-D identification could be due to a PPV-M and PPV Rec more efficient transmission by vectors and a best adaptation in hosts (James et al., 2013).

Conclusions

According to the European regulation that ranked PPV as quarantine pest, sharka was subjected to a national monitoring and eradication programme until 2021, whereas nowadays, with the new European regulation that downregulated PPV to RNQP due to its endemicity, the management of sharka in Italy is demanded of farmers. However, information collected in the last decades on the diffusion of sharka in Italy show scattered results, incomplete and difficult to interprete. This review summarized the the development and spread since the first identification of its causal agent occurred around fifty years ago and summarised the monitoring activity of the last decade in Tuscany. Data retrieved from a variety of sources (e.g., published literature, official documents and personal communications) showed that (i) sharka spread across almost the whole Italian peninsula as only the Liguria, Umbria and Aosta Valley regions remain disease-free, (ii) the regions with higher fractions of infected districts are not always those more dedicated to the production of stone fruits; (iii) only the three major PPV strains causing sharka, i.e., PPV-D, PPV-M and PPV-Rec, have been reported in Italy; and (iv) only apricot, peach and plum (i.e., widespread and economically relevant species) were reported as PPV hosts in Italy (with different rates of occurrence among regions). In addition, the analysis of the data from Tuscany showed that (i) sharka has been reported since the 1990s, but extensive PPV monitoring campaigns were run from 2013 to 2021, especially in nurseries; (ii) higher number of symptomatic and PPV positive samples were recorded in farms, mostly in the Arezzo and Florence districts, important stone fruit growing regions, and (iii) only PPV-M and PPV-Rec strains seem still present. We believe that the present overview will benefit both researchers for future investigations on sharka and farmers that have to manage the disease.