J. Hortl. Sci. Vol. 17(2) : 488-495, 2022 This is an open access article d istributed under the terms of Creative Commons Attribution-NonCommer cial-ShareAl ike 4.0 International License, which permits unrestricted non-commercial use, d istribution, and reproduction in any med ium, provide d the original author and source are credited. Original Research Paper INTRODUCTION Plum (Prunus spp.) is one of the most commercially important fruit species in Iran. Plums are temperate zone fruits, but they are widely grown throughout the world, from the cold climate of Siberia to the sub- tropical conditions of the Mediterranean region (Son, 2010). Prunus species such as P. cerasifera, P. domestica, P. institia and P. Salicina are widely grown thr oughout the wor ld. T he Eur opean plum ( P. domestica) and the Japanese plum (P. salicina) are more important in terms of commercial production (Ozbek, 1978). Grafting is largely used in the production of vegetable and fruit-bearing crops in order to increase uniformity, vigor, and adaptation to biotic and abiotic stresses. The compatibility of rootstock and scion plays a crucial role in establishing highly efficient root systems through grafting (Goldschmidt, 2014; Warschefsky et al., 2016). However, this trait varies significantly even between closely related species, which necessitates the evaluation of compatibility before grafting a specific scion genotype into the rootstock. For the stone fruit industry that heavily relies on vegetatively propagated cultivars (i.e., individual genotypes) via grafting, the long-term vitality of the union between the rootstock and scion is crucial (Lee et al., 2011; Guan et al., 2012). Graft incompatibility generally occurs at the early sta ge of gra ft development when the va scula r connection is forming. However, symptoms may manifest at large growth stages such as low plant development related to physiological differences in the stem diameter, which impairs the normal flow of photoassimilates and the lignification of grafted tissues (Souza et al., 2018), thus decreasing the hydraulic conductivity of the graft union (Tworkoski and Fazio, 2015). These symptoms appear during the plant fruiting period when the plant is subjected to a high demand for water transport (Martinez-Ballesta et al., 2010). Incompatibility does not permanently become Possibility of early detection of graft incompatibility in some commercial plum cultivars by phenolic compounds analysis Arghavan S.1, Ganji Moghadam E.2*, Fahadan A.1, Zamanipour M.3 1Department of Horticulture, Azad University Branch Shirvan, North Khorasan, Iran 2Crop and Horticultural Science Research Department, Khorasan Razavi Agricultural and Natural Resources Research and Education Center, AREEO, Mashhad, Iran 3Department of Agriculture, Technical and Engineering Faculty, Velayat University, Iranshahr, Iran *Corresponding author Email : eganji@hotmail.com ABSTRACT The incidence of incompatibility signs in the grafting point can be delayed, and the analysis of phenols is used as an applicable early sign for the detection of graft incompatibility. Accordingly, this study mainly aimed to investigate compatibility/incompatibility in 10 commercial plum cultivars grafted on myrobalan and apricot rootstocks, followed by determining the role of phenols in graft incompatibility. The evaluated cultivars included Santarosa, Ghatreh tala, Shams, Dargazi, No. 16, No. 17, Laroda, Simka, Bokhara, and Stanley. The results showed significant differences in the stem diameter. The union graft location in Shams, Laroda, Simka, Stanley, and Ghatreh tala cultivars on apricot rootstock was thicker than the scions and stocks. Phenolic compounds in the union graft decreased in all plum cultivars on myrobalan rootstock in comparison with other sites. Finally, the most phenolic accumulation belonged to the union graft on Santarosa, Ghatreh tala, and Shams on apricot rootstocks. Therefore, it seems that phenolic compounds in plums can be used as a biochemical marker in graft incompatibility. Keywords: Apricot rootstock, incompatibility, myrobalan rootstock, phenolic content, plum 489 Possibility early detection of graf incompatibility in plum cultivars J. Hortl. Sci. Vol. 17(2) : 488-495, 2022 apparent immediately after grafting. It may take several years to manifest failure with establishing graft-union leading to major economic losses to growers and nurseries. In addition, the significant delay in the appearance of incompatibility symptoms renders the evaluation and transfer of new fruit tree genotypes to industry time-consuming, expensive, and laborious (Gainza et al., 2015; Pina et al., 2017). Fruit trees are typically formed by a combination of the scion and rootstock. A good union between a scion a nd r ootstock is necessa r y for a successful combination (Errea et al., 2001). Graft incompatibility symptoms in woody species include bark thickening in the connection region, chlorotic leaves, premature leaf fall, budding delay, vigor differences between the rootstock and scion, excessive stem thickening below, above, or at the point of the graft union. Other symptoms a re gr a ft union disr uption, r educed vegetative growth, low productivity, and premature plant death (Zarrouk et al., 2010; Hartmann et al., 2011). The grafted partners frequently belong to the same species or genus although the use of genetically divergent genotypes is also common. Incompatibility repeatedly occurs in the plum when it is grafted on other Prunus species such as the apricot graft. Different reasons may influence gr aft success, including the inher ent system of cellula r incompatibility, the formation of plasmodesmata, vascular tissue connections, and the presence of growth regulators and peroxidases (Usenik et al., 2006). Macromolecules (phloem proteins, RNA, and hormones) that are present in the sap phloem might also be important during vascular differentiation in the compatibility process (Pina and Erea, 2005). Different methods for an early detection of graft incompatibility have already been used, including in vitro techniques (Errea et al., 2001), isozyme analysis (Fernandez- Garcia et al., 2004; Gulen et al., 2002), and phenol analysis (Musacchi et al., 2000). Such compounds are important to the early growth stages of connections between scion-rootstock combinations since the cell wa lls of xylem tissues a re dynamic str uctures composed of polysaccharides, phenolic compounds, miner a ls, a nd proteins (Her r er o et al. , 2014). Moreover, the presence of phenolic compounds has been identified as an important marker for the evaluation of graft compatibility between scions and rootstocks (Prabpreea et al., 2018). The analysis and recognition of structural phenol diversity are of particular interest because of their physiological roles during the first steps of graft establishment (Usenik et al., 2006). The presence of phenols was generally associated with small cells in incompatible combinations, which did not lead to successful unions (Er rea et al., 2001). Higher concentrations of catechin and epicatechin were found in quince-incompa tibility cultiva r s befor e the appearance of visible incompatibility symptoms (Musacchi et al., 2000). In less compatible apricot combination higher level of flavanols, catechin, and epicatechin, was characteristics (Errea et al., 2000). In several apricot combinations grafted on prunus rootstocks, graft incompatibility resulted in breakdown of the trees at the union years after planting, therefore an early selection process could help in detecting a comparatively compatible combination. Analysis of the phenol content at the graft union can be used as a technique for the estimation of graft incompatibility (Dogra et al., 2018). Several studies have shown that phenolic compounds in incompatible combinations move from vacuole to cytoplasm and cause inhibition of lignification which is required during early stages of establishment of scion–stock connections. The cell wall of xylem vessels are dynamic in nature composed of phenolic compounds (for exa mple, lignins), miner a ls, polysaccharides and proteins (Liu, 2012; Herrero et al. , 2014). Pla nt hor mones, especia lly a uxins determine the compatibility of a rootstock-scion combination by interacting with phenolic compounds. Incompatibility has been associated with increased levels of phenolic compounds above the graft union which adversely affect the auxin transport (Errea, 1998). Low auxin concentration in incompatible combinations in turn affect the differentiation of vascular tissues and lignification (Aloni, 2010; Koepke and Dhingra, 2013). All these changes will lead to the formation of weak unions which may cause huge economic losses to the growers. More information about the compounds responsible for inducing graft incompatibility is needed (Gainza et al., 2015). Given the above-mentioned explanations, the current study mainly sought to evaluate the relationship between graft incompatibility and the total phenolic content in some commercial plum cultivars, as well as to determine whether such analysis can be a useful tool for the early detection of graft incompatibility. 490 Moghadam et al MATERIALS AND METHODS Plant material T his r esea r ch wa s conducted a t a t Golma ka n Horticultural Research Station (59° 17' N; 36° 32' E), north east of Iran/Mashhad, with an average altitude of about 1176 m. The mean temperature for growing season was 13. 4°C and tota l seasonal precipitation was 239.7 mm. The nursery soil was sandy loam with low organic matter. Drip irrigation was applied in the nursery. The trees were planted at a spacing of 100 × 10 cm (100.000 trees ha-1) and budded (T-budding technique) 10 cm above the gr ou nd leve l. All r oot s t oc ks ( a p r ic ot a nd myrobalan) were seedlings, and the samples were taken from 1-year-old plum trees. The content of total phenols above, below, and at the union graft in 10 plum cultivars (i.e., Santarosa, Ghatreh tala, Laroda, Stanley, Dargazi, No. 16, No. 17, Bokhara, Sha ms, and Simka) gra fted on myroba la n and apricot seedling rootstocks was analyzed as well. Field study Trees were used one year after grafting for the study. The stem diameters of scions, stocks, and the graft union were measured using a pair of caliper. The units of measurment was to mm. Phenol extraction Three trees from each grafting combination were analyzed, and the samples were collected in June. The small sections of the bark above, below, and at the union graft (1 cm above and below the graft union, 1.5 cm in length) were removed with a knife and immediately frozen in liquid nitrogen. Phloem with cambium was used for analysis. T he s a mp le s wer e ex t r a c t ed wit h a 1 . 5 ml methanol-acetone-water solution (7:7:1 v/v/v). In a mor t a r, 5 0 mg of t he p la nt ma t er ia l wa s homogenized with a 1.5 ml extraction solution. Next, the samples were centrifuged at 6000Xg for 20 min using a bench centrifuge. Then, the solvents were evaporated in rotary at 40 ÚC, and the residue was dissolved in 5 ml of deionized water. The extracts were stored at -80 ÚC until the analysis of the total phenolic content (Mngomba et al., 2008). The applied chemical reagents were obtained from Merck Company. Total phenolic content analysis The amounts of the total phenol content in pulm cultivar extracts were determined with the Folin- Ciocalteau reagent using the method of Spanos and Wrolastad (1990), as modified by lister and Wilson (2001). To this end, 0.5 ml of Folin-Ciocalteau reagent and 2 ml of Na2CO3 (7.55/a, w/v) were added to 100 µl of each sample (three replicates) and then incubated at 45 ÚC for 15 min. The absorbance of all samples was measured at 620 nm using a SPECTRA max- PLU5384 UV-Vis spectrophotometer. The results were expressed as milligrams of catechol acid equivalent per gram of dry weight (Ganji Moghadam et al., 2007). Statistical analysis The trial was laid out in a factorial experiment based on completely r a ndomized design with thr ee replications where each replication contained 10 trees. Factors a contains cultivars in 10 levels (Santarosa, Ghatreh tala, Laroda, Stanley, Dargazi, No. 16, No. 17, Bokhara, Shams, and Simka), factor b contains rootstock in 2 levels (myrobalan and apricot seedling) and Factor c contains 3 levels (above, below, and at the union graft). Three replicates of each sample were used for statistical analysis using MSTAT-C, version 1.42. Data were subjected to the analysis of variance, and means were compared by the least significant difference. Differences at P<0.05 were considered statistically significant. RESULTS AND DISCUSSION Significa nt differences in stem diameters were observed above, below, and at the union graft. The stem diameters below the graft unions were visibly greater than those of above and the union graft on myr oba la n r ootstock and Sa nta r osa , Da rga zi, Bokhara, No. 16, and No.17 cultivars on the apricot rootstock. The unions were thicker than scions and stocks in Ghatreh tala, Shams, Laroda, Stanley, and Simka on the apricot rootstock (Table 1). In the study of the independent effect of the total phenol content in the union graft, the highest total phenolic content was detected in the below graft union while the lowest content was found in the above graft union. Above and union graft differences were not significant (Figure 1a). Based on the evaluation of the effect of the union graft in apricot and myrobalan rootstocks, the highest and J. Hortl. Sci. Vol. 17(2) : 488-495, 2022 491 Table 1 : Thickness (mm) above, below, and at union graft of different plum cultivars grafted on apricot and myrobalan rootstocks Graft Combination Above the Union At the Union Below the Union Apricot rootstock Santarosa 6.82* 11.95a 12.37a Ghatreh tala 8.2c 16.08a 11.57b Shams 7.24a 9.09a 7.93a Laroda 5.8b 11.30a 10.95a Dargazi 7.15c 12.98b 16.18a Simka 5.16b 11.79a 9.21a Bokhara 5.9c 10.27b 11.86a Stanely 6.86a 13.72a 11.11a No. 16 6.03b 12.13a 14.41a No. 17 5.03b 11.62ab 18.21a Myrobalan rootstock Santarosa 6.93b 12.71b 20.55a Ghatreh tala 8.41c 11.57b 16.84a Shams 6.76b 10.23b 17.74a Laroda 7.94c 12.16b 16.38a Dargazi 9.53c 13.49b 18.48a Simka 8.22c 13.61b 19.02a Bokhara 7.00c 9.28b 11.31a Stanely 8.41b 13.67a 16.99a No. 16 7.18b 10.88b 19.44a No. 17 6.83b 11.23b 15.11a Note : *Means with the same letters within a row are not significantly different at P<0.05. the lowest total phenolic contents were observed in the below gr a ft union on myr oba la n a nd a pr icot rootstocks, respectively (Figure 1b). The highest total phenolic content was detected in the below graft union of Laroda, Shams, Stanley, Santarosa, and Dargazi cultivars grafted on the myrobalan rootstock whereas the lowest content was found in the below graft union Fig. 1 : Effects of Independent Union Graft (a) and Interaction Rootstocks and Graft Union (b) on the Total Phenolic Content (mg Catechol Acid Equivalent per g of Dry Weight) Possibility early detection of graf incompatibility in plum cultivars J. Hortl. Sci. Vol. 17(2) : 488-495, 2022 492 of Shams, Laroda, Ghatreh tala, and Santarosa cultiva rs gr afted on the a pricot rootstock. The compared differences in the total phenol content in the union and below graft demonstrated the significant accumulation of phenol in the union graft in Santarosa, Ghatreh tala, Laroda, Stanley, Dargazi, Bokhara, Shams, and Simka cultivars grafted on the apricot rootstock while it decreased on myrobalan rootstock (Table 2). The stem diameters below the graft unions were visibly greater compared to the above and at union graft on myr oba la n r ootstock and Sa nta r osa , Da rga zi, Bokhara, No. 16, and No.17 cultivars on the apricot rootstock. The unions were thicker than the scions and stocks in Ghatreh tala, Shams, Laroda, Stanley, and Simka on the apricot rootstock. The highest total phenolic contents wer e detected in myroba la n rootstocks while the lowest contents were found in apricot rootstocks. The composition of phenols depends on the genetic constitution of the plant species, and hence, some plants accumulate more than others. These results are in agreement with those of Pina ane Errea (2005) indicating that some apricot cultivars grafted onto a plum rootstock demonstrated only some callus differentiation occurred on cambium and vascular tissues while a large portion of the callus never demonstrated a differentiation. This interrupts va scula r connections beca use of the la ck of differentiation that brings discontinuities in the ca mbium a nd the for ma tion of a ba nd of Moghadam et al Table 2 : The Amount of the total phenol content (mg gallic acid equivalent per g of dry weight) in above, below, and at the union graft of different plum cultivars grafted on apricot and myrobalan rootstocks Graft Combination Above the Union At the Union Below the Union Apricot rootstocks Santarosa 1033.79a 1274.88a 441.01b Ghatreh tala 1051.14b 1905.93a 430.14b Shams 1010.95a 1424.65a 317.81b Laroda 810.05a 902.28a 401.82a Dargazi 1114.15a 1302.28a 747.94a Simka 1166.21a 1513.24a 839.27a Bokhara 677.17a 951.59a 555.25b Stanely 762.56a 1250.23a 698.63a No. 16 925.15b 1135.16a 1091.33ab No. 17 807.31b 1347.91a 1204.56a Myrobalan rootstocks Santarosa 611.78b 363.47b 2230.13a Ghatreh tala 1421.91a 663.93b 1476.86a Shams 805.47b 1112.32b 2413.69a Laroda 1378.99b 536.07b 3215.52a Dargazi 830.14b 449.31c 1221.46a Simka 1053.88b 763.47b 1789.95a Bokhara 838.36b 989.04b 1813.69a Stanely 1120.59b 1114.15b 2291.33a No. 16 629.23c 1309.59b 1882.19a No. 17 1828.31a 619.18b 2122.51a Note : *Means with the same letters within a row are not significantly different at P<0.05. J. Hortl. Sci. Vol. 17(2) : 488-495, 2022 493 parenchymatous cells. Based on the findings regarding the evaluation of the independent effect of the total phenol content in the union graft, the highest and lowest total phenolic contents were detected in the below and above graft unions, respectively. The results related to the effect of the union graft on apricot and myrobalan rootstocks, the highest and lowest total phenolic contents belonged to below graft union on myr oba la n r ootstock a nd a pr icot r ootstock, respectively. Mngomba et al. (2008) reported that the accumulation of phenol deposits at the place of the graft union might inhibit graft compatibility. Usenik et al. (2006) also demonstrated that differences in phenol accumulation below and above the graft union might serve as an indicator of incompatibility. The highest total phenolic content was detected below the graft union of Laroda, Shams, Stanley, Santarosa, and Dargazi cultivars grafted on myrobalan rootstock whereas the lowest content was found in the below graft union of Shams, Laroda, Ghatreh tala, and Santarosa cultivars grafted on apricot rootstock. The comparison of differences in the total phenol content in union and below graft showed the significant accumulation of phenol in the union graft in Santarosa, Ghatreh tala, Laroda, Stanley, Dargazi, Bokhara, Shams, and Simka cultivars grafted on a pricot rootstock while it decreased on myrobalan rootstock. In apricot/plum combinations, a high concentration of phenolic compounds was observed in undifferentiated callus at the scion-rootstock interface of plants previously categorized as incompatible (Pina et al., 2012), and thus they are involved in the processes of differentiation of vascular tissues (Usenik et al., 2006), which is in line with our results. The statistically significant accumulation of phenol in the graft union was ascertained in Santarosa, Ghatreh tala, Laroda, Stanley, Darga zi, Bokhar a, Shams, and Simka cultivars grafted on apricot rootstock when compared with the content below the graft union while phenol above the graft union decreased in plum cultivars on myrobalan rootstock. The highest accumulation of phenol in the union graft that can be used as a biochemical marker of graft incompatibility are observed in Ghatreh tala, Shams, and Santarosa on apricot rootstock, which corroborates with the findings of Prabpreea et al. (2018), implying that the presence of phenolic compounds has been identified as an impor ta nt ma r ker for the eva lua tion of gr a ft incompatibility between scion and rootstocks in the union graft. CONCLUSION The early phase of graft incompatibility is complex and needs further evaluation. 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Changes in cell/ tissue organization and peroxidase activity as ma r ker s for ea r ly detection of gr a ft incompatibility in peach/plum combinations. J. Am. Soc. Hortic. Sci., 135(1): 9-17. Possibility early detection of graf incompatibility in plum cultivars J. Hortl. Sci. Vol. 17(2) : 488-495, 2022 (Received : 27.07.2021; Revised : 18.03.2022; Accepted : 15.09.2022)