Abstract
Physalis peruviana L. crops are exposed to different stress conditions that limit their productivity. Within these conditions, abiotic stress caused by water and biotic stress by Fusarium oxysporum f. sp. physali (Foph) are frequent at commercial levels. The foliar application of synthetic elicitors can be a tool to mitigate the negative impacts of these stresses. The objective of this study was to evaluate the interaction between Foph inoculation and three foliar applications of brassinosteroids (BR), salicylic acid (SA), and a commercial elicitor based on botanical extracts (BE) of Echinacea purpurea, Potentilla erecta, and Aloe vera on the physiological [stomatal conductance (gS), leaf water potential (Ψwf), chlorophyll fluorescence, and growth] and biochemical [photosynthetic pigments, malondialdehyde (MDA) production, and proline content] responses of cape gooseberry plants subjected to a 6-day waterlogging period. The established treatments were as follows: 1) waterlogged plants without Foph; 2) waterlogged plants with Foph; 3) waterlogged, noninoculated (Foph−) plants treated foliarly with BR, SA, or BE; and 4) waterlogged, inoculated (Foph+) plants treated foliarly with BR, SA, or BE. The results showed that the foliar application of BR or SA reduced vascular wilt development in plants subjected to a hypoxia period. In addition, three applications of BR, SA, or BE favored gS, Ψwf, growth, and chlorophyll fluorescence parameters in cape gooseberry plants under the interaction between Foph and oxygen deficit in the soil. Also, higher photosynthetic pigment and proline contents were observed in plants treated with elicitors under stress combination, whereas a lower MDA production was evidenced in this group of plants. In conclusion, BR, SA, or BE can help mitigate the negative effects of the simultaneous occurrence of Foph and a waterlogging condition for 6 days in cape gooseberry plants.
Cape gooseberry (P. peruviana L.) is an herbaceous plant from the South American Andes that belongs to the Solanaceae family. P. peruviana is the second exported fruit species in Colombia with an export value of US$27.8 million during 2017 (Álvarez-Flórez et al., 2017; Olivares-Tenorio et al., 2017). Also, this crop occupied 1023 ha with a production of ≈15,586 t in 2017 (Agronet, 2019; Procolombia, 2019).
P. peruviana crop productivity has decreased in Colombia during recent years because of factors such as vascular wilt (Foph), abiotic stresses (waterlogging), and/or the interaction between these factors (Aldana et al., 2014; Moreno-Velandia et al., 2019; Villarreal-Navarrete et al., 2017). Vascular wilt is the most limiting crop disease that has been reported in more than 50% of growing areas in the country, generating yield reductions or total crop loss (Osorio-Guarín et al., 2016; Simbaqueba et al., 2018). Disease symptoms include marginal leaf chlorosis, vascular tissue browning, plant wilting, atrophy, and eventual death (Abdallah et al., 2016). Pathogen infection occurs by direct penetration and intracellular growth of hyphae through the root tip into the xylem vessels, causing plant wilting (Król et al., 2015). Disease management has been hampered by the resistance of the pathogen to commercial fungicides. In addition, the presence of chlamydospores allows the prolonged survival of the pathogen, which can infect roots of new plants (Król et al., 2015; Osorio-Guarín et al., 2016).
Crops are currently facing waterlogging conditions (hypoxia) because of high rainfall, inefficient irrigation practices, and/or inadequate soil drainage, generating growth and yield limitations (Herzog et al., 2016). Waterlogging stress can cause several types of physiological responses in plants and also can favor the incidence of diseases (Rao and Li, 2003). Short or moderate waterlogging periods can cause low root growth and dry matter accumulation, leaf senescence, plant wilting, and crop death (Wu et al., 2015). Leaf gas exchange properties (gS, transpiration, and photosynthesis) and photosynthetic pigment content also are associated with the type of plant acclimation responses (Zhu et al., 2016). In addition, MDA and proline production have been used as biochemical markers to characterize plant responses to abiotic and biotic stresses (Dar et al., 2016; Irulappan and Senthil-Kumar, 2018).
Chlorophyll fluorescence parameters also are affected by hypoxia conditions, and these parameters can be effective in detecting changes in the mechanisms involved in plant acclimation (He et al., 2018; Shao et al., 2013). A low electron transport rate (ETR), photochemical efficiency of photosystem II (PSII) (Fv/Fm), photochemical quenching (qP), and a high nonphotochemical quenching (NPQ) have been reported under waterlogging conditions (Liu et al., 2014; Wu et al., 2015). Moderate periods of hypoxia (6–8 d) also have caused a reduction in plant height, leaf area (LA), plant dry weight, and high plant wilting in cape gooseberry plants (Aldana et al., 2014).
Waterlogging also can increase plant diseases associated with soil pathogens, such as vascular wilt caused by F. oxysporum f. sp. cubense in banana (Musa spp.) (Aguilar et al., 2000; Shivas et al., 1995), crown and root rot caused by Phytophthora spp. in apple (Malus ×domestica Borkh.) and raspberry (Rubus idaeus L.) (Duncan and Kennedy, 1989; Wilcox, 1993), and damping-off caused by Pythium irregulare in beans (Phaseolus vulgaris L.) (Li et al., 2015b). This greater plant susceptibility to soilborne pathogens under waterlogging conditions is associated with the ability of microorganisms to grow in anaerobic conditions (Rao and Li, 2003). Regarding the combined stress effect (waterlogging and plant pathogen), Moslemi et al. (2018) observed greater basal leaf chlorosis, wilting, and necrosis in pyrethrum plants [Tanacetum cinerariifolium (Trev.) Schultz. Bip.] infected with Paraphoma vinacea, F. oxysporum, and Fusarium avenaceum exposed to waterlogging for 7 d. Also, these authors reported that hypoxia conditions generated a lower plant biomass, and lower stem and flower number in pathogen-infected plants.
The use of synthetic elicitors can be considered an effective tool to mitigate the negative effects generated by abiotic and biotic stresses in plants (Llorens et al., 2017; Naik and Al-Khayri, 2016). Elicitors are chemical compounds that can be sprayed on leaves, causing a stimulus on plant defense mechanisms and secondary metabolite synthesis under abiotic and biotic stress conditions (Llorens et al., 2017; Ramírez-Godoy et al., 2018; Thakur and Sohal, 2013). SA, BR, and plant BEs have been studied and characterized as compounds that activate plant defense mechanisms against stress conditions (abiotic and biotic) (Bektas and Eulgem, 2015; Singh et al., 2017; Vardhini and Anjum, 2015; Xue et al., 2013; Zhang et al., 2015).
SA acts as a signaling molecule modulating tolerance to stress through the activation or regulation of physiological, biochemical, and molecular processes (Bernal-Vicente et al., 2017; Khan et al., 2015). Foliar SA application decreased the size of the lesion generated by Phytophthora cinnamomi in lupin (Lupinus augustifolius) roots (Groves et al., 2015) and enhanced growth and physiological and biochemical behavior of tomato plants (Solanum lycopersicum L.) with waterlogging for 45 d (Singh et al., 2017).
BRs are polyhydroxylated steroidal plant hormones that also can help the tolerance to different abiotic and biotic stresses in plants (Anwar et al., 2018; Fariduddin et al., 2014). BR application decreased the negative effects generated by Verticillium dahliae in cotton plants (Gossypium hirsutum L.) (Bibi et al., 2014) and improved protein content, dry matter yield, nitrogen uptake, and harvest index in maize plants (Zea mays L.) with waterlogging for 10 d (Otie et al., 2019).
BEs also have been considered as an effective alternative for plant pathogen control and stress mitigation in recent years (Joseph et al., 2017; Van Oosten et al., 2017). Rongai et al. (2017) observed that BE from pomegranate (Punica granatum) peels showed antifungal activity on F. oxysporum f. sp. lycopersici in tomato plants (S. lycopersicum L.) under in vitro conditions. Elansary et al. (2017) also observed a positive effect of seaweed BE sprays on the physiological and biochemical traits of seashore paspalum (Paspalum vaginatum) plants subjected to water stress.
Foph management practices in cape gooseberry crops have been mainly based on the use of synthetic fungicides (Moreno-Velandia et al., 2019); however, synthetic elicitors have been used as alternatives for soilborne pathogen management in recent years (McGovern, 2015). Studies about synthetic elicitors have been focused separately on disease control (Ding et al., 2009a; Mandal et al., 2009; Mostafa et al., 2018) or their effect on abiotic stress mitigation (Csiszár et al., 2018; Mansori et al., 2015; Rao and Dixon, 2017); however, the available literature on the use of these compounds to reduce the negative impact generated by combined stresses (pathogens and abiotic stresses) in Andean fruit trees, such as cape gooseberry, is still scarce. The present research hypothesizes that foliar BR, SA, or BE sprays can help to mitigate the negative effects caused by these two stresses (Foph and waterlogging) by enhancing physiological (gS, Ψwf, chlorophyll fluorescence parameters, and growth) and biochemical (proline, MDA, and photosynthetic pigments) responses in cape gooseberry plants.
Materials and Methods
Growth conditions and pathogen inoculation.
An experiment was carried out from Sept. 2018 to Jan. 2019 under greenhouse conditions at the Faculty of Agricultural Sciences of the Universidad Nacional de Colombia, Bogotá (lat. 4°35′56″N, long. 74°04′51″W, altitude 2557 m above sea level). The general environmental conditions during the experiment were as follows: natural photoperiod of 12 h (photosynthetically active radiation of 1500 μmol·m−2·s−1 at noon), ≈65% relative humidity, 28.4/12.5 °C day/night temperature, and 20.5 °C average temperature. Two-month-old ecotype ‘Colombia’ (P. peruviana L.) seedlings purchased from a local nursery were used. To rule out F. oxysporum infection, the plants were previously indexed using the methodology described by Leslie and Summerell (2006). Then, seedlings were subjected to an acclimation period for 15 d. When plants developed between three and four true leaves, they were transplanted into 2-L plastic pots, containing a soil-based substrate (clay loam) and rice husk (3:1 v/v) with and without Foph inoculum. Before substrate inoculation, the methodology described by Park (1961) was used to confirm Foph absence in the soil used for the substrate mixture.
Substrate inoculation was performed by adding 100 mL of a liquid Foph suspension at a concentration of 1 × 106 microconidia/mL per 0.9 kg of substrate (soil + rice husk), guaranteeing a final concentration of 1 × 104 microconidia/g of substrate (Osorio-Guarín et al., 2016). Finally, two inoculation conditions were obtained (with and without Foph presence). The Foph-Map5 strain supplied by the Biological Control Laboratory of the Corporación Colombiana de Investigación Agropecuaria (Agrosavia, Mosquera, Colombia) was used as a source of pathogen inoculum in the present experiment. Young mycelium segments of the supplied strain were cultured in 50 mL potato dextrose broth (Difco, Becton Dickinson, Sparks, MD) in 250-mL Erlenmeyer flasks and incubated for 7 d with constant agitation in an orbital shaker (Laboratory-Line, Melrose Park, IL) at 125 rpm and 28 °C under dark conditions (Moreno-Velandia et al., 2019).
Seedlings were irrigated daily with 50 mL of a nutrient solution prepared from a complete liquid fertilizer (Nutriponic; Walco SA, Bogotá, Colombia) at a dose of 5 mL·L−1 H2O from transplanting to the beginning of the waterlogging periods, and later from the end of the natural drainage to the end of the experiment. The concentration of the nutrient solution was as follows: 2.08 mm Ca (NO3)2·4 H2O, 1.99 mm MgSO4·7 H2O, 2.00 mm NH4H2PO4, 10.09 mm KNO3, 46.26 nM H3BO3, 0.45 nM Na2MoO4·2 H2O, 0.32 nM CuSO4·5 H2O, 9.19 nM MnCl2·4 H2O, 0.76 nM ZnSO4·7 H2O, and 19.75 nM FeSO4·H2O. The water volume used was obtained by daily quantification of the evapotranspiration needs of the plants by means of the gravimetric technique described by Hainaut et al. (2016).
Waterlogging and synthetic elicitor treatments.
At the time of transplantation, two groups of 40 plants each were obtained: the first group consisted of seedlings planted in substrate with Foph (inoculated), and the second corresponded to seedlings planted in substrate without Foph (noninoculated). Then, the two groups were subjected to a waterlogging period of 6 consecutive d. The stress condition due to waterlogging was imposed by placing the seedlings inside 120-L plastic boxes, to which 60 L tap water was added to guarantee a 5-cm level on the base of the stem 5 d after inoculation (DAI). At the end of the waterlogging period (11 DAI), the seedlings were removed from this condition and natural drainage was allowed until reaching the field capacity in the substrate (18 DAI). Afterward, the seedlings were maintained under normal irrigation conditions until the end of the experiment (51 DAI).
A group of 10 plants was selected to be sprayed with SA, BR, or BE (a commercial product based on E. purpurea, P. erecta, and A. vera extracts). The doses of each synthetic elicitor were 100 ppm, 1 ppm, and 2.5 mL of the commercial product per liter of H2O, respectively. Eight different groups of treatments were obtained depending on Foph inoculation, waterlogging condition, and synthetic elicitor spray, which are summarized as follows: 1) waterlogged plants without Foph; 2) waterlogged plants with Foph; 3) waterlogged, noninoculated (Foph−) plants sprayed with BR, SA, or BE; and 4) waterlogged, inoculated (Foph+) plants sprayed with BR, SA, or BE. Likewise, two additional groups with and without Foph inoculation, without waterlogging, and without synthetic elicitors sprays were established as absolute control (Foph−) and pathogen control (Foph+). The general characteristics of the synthetic elicitors are presented as follows: SA (2-Hydroxybenzoic acid; Panreac Applichem, Barcelona, Spain); Biomex DI-31 [(25 R) 3β,5α-dihydroxy-spirostan-6-one; Minerales exclusivos SA, Bogotá, Colombia]; Loker (E. purpurea, P. erecta, and A. vera extracts, K and Mg salts; Biolchim S. p. A., Medicina, Bologna, Italy).
Foliar synthetic elicitor applications were performed at three different times during the experiment: 1) foliar application 8 d before inoculation, 2) foliar application at the time of inoculation, and 3) foliar application 8 DAI. In general, each synthetic elicitor spray was carried out between 0700 and 0900 hr, using a 1.8-L manual spray pump (Royal Condor Garden, Soacha, Colombia) with an application volume of 20 mL H2O per plant, wetting the upper and lower leaf surfaces. A coadjuvant [Tween 20 (Merck, Darmstadt, Germany)] was used at a rate of 0.02% (v/v) in all foliar applications. Control plants were sprayed with distilled water and the adjuvant at the same concentration. The length of the waterlogging period, number of foliar applications, and doses used for each elicitor were determined from previous studies (Chávez-Arias et al., 2019). A total of 10 treatment groups were obtained and arranged in a completely randomized design in which each treatment consisted of 10 plants (repetitions). Finally, the experiment lasted 74 d.
Analysis of vascular wilt severity.
where n is the level of infection according to the scale, v is the number of plants present in each level, and V is the total number of evaluated plants.
where n is the number of evaluations, yi and yi+1 are the values of the severity scale at evaluation time, and
Finally, pathogen presence or absence in Foph-inoculated and noninoculated plants was confirmed by isolates in potato dextrose agar (PDA) medium (Oxoid, Basingstoke, UK) from explants taken from the base of the stem at each evaluation time (11 and 51 DAI) (Leslie and Summerell, 2006).
gS and Ψwf.
gS and Ψwf were estimated on the fourth fully expanded leaf from the upper portion of the canopy. A steady-state porometer (SC-1; Decagon Devices Inc., Pullman, WA) was used to estimate gS. Then, Ψwf was measured with a Scholander pressure chamber (Model 615; PMS, Corvallis, OR) on the same leaf used to estimate gS on completely sunny days at 11 and 51 DAI between 0900 and 1200 hr.
Chlorophyll fluorescence parameters.
The same leaves used to estimate gS were used for the measurement of maximum quantum yield of PSII (Fv/Fm), qP, NPQ, and ETR using a modulated fluorometer (MINI-PAM; Walz, Effeltrich, Germany). Before taking the measurements, leaves were adapted to darkness using the fluorometer’s clips for 10 min. Then, leaves received a pulse of actinic light of up to 2600 μmol·m−2·s−1 on their surface to obtain the fluorescence parameters. These measurements were also taken at 11 at 51 DAI.
Growth parameters.
Leaf photosynthetic pigments.
The equations described by Wellburn (1994) were used to estimate total chlorophyll (TChl) and carotenoid (Cx+c) contents. Leaf samples of 30 mg from the middle third of the canopy were collected and then homogenized in 3 mL of 80% acetone. Then, the samples were centrifuged (centrifuge model 420101; Becton Dickinson Primary Care Diagnostics, Sparks, MD) at 5000 rpm for 10 min to remove particles. The supernatant was diluted to a final volume of 6 mL by adding acetone (Sims and Gamon, 2002). Chlorophyll content was determined at 663 and 646 nm, and carotenoids were measured at 470 nm using a spectrophotometer (Spectronic BioMate 3 ultraviolet-vis; Thermo, Madison, WI).
Proline and MDA content.
The thiobarbituric acid method described by Hodges et al. (1999) was used to estimate membrane lipid peroxidation (MDA). Leaf samples of 300 mg from the middle third of the canopy of plants from the different treatments were macerated and stored in liquid nitrogen. Samples were centrifuged at 5000 rpm for 10 min and their absorbances were estimated at 440, 532, and 600 nm with the spectrophotometer. Finally, an extinction coefficient (157 M·mL−1) was used to obtain the MDA concentration. Proline and MDA were measured at 51 DAI.
Experimental design and data analysis.
Data were analyzed by a factorial arrangement with inoculation with the pathogen (with and without Foph) as the first factor, and synthetic elicitors (SA, BR, or BE) as the second factor. Each treatment group consisted of 10 plants. A principal components analysis was performed using the InfoStat 2016 program (analytical software; Universidad Nacional de Cordoba, Córdoba, Argentina) to select the best synthetic elicitors under the interaction between waterlogging and F. oxysporum f. sp. physali (Foph) inoculation. Then, the selected treatments were compared with the absolute control (Foph−) and pathogen control (Foph+) through a completely randomized analysis. An analysis of variance was performed in all cases, and when significant differences (P ≤ 0.05) were found, a Tukey post hoc test was used for means comparison. The percentage values were transformed using the arcsine function. Data were analyzed using the Statistix v 9.0 software (Analytical Software, Tallahassee, FL). The figures and cluster analysis were carried out using the software SigmaPlot (version 12.0; Systat Software, San Jose, CA).
Results
Vascular wilt severity expressed as AUDPC and disease index.
The evaluation of the AUDPC and vascular wilt index showed differences at P ≤ 0.001 between plants of all Foph-inoculated treatments at 51 DAI. Foph presence was confirmed by isolates in PDA from affected material (Fig. 1). The pathogen was not isolated from plants without inoculation, without any synthetic elicitor sprays, without any stress, or from plants with only waterlogging (Fig. 1A).
Leaf wilting and vascular browning of cape gooseberry plants with and without Fusarium oxysporum f. sp. physali (Foph) inoculation under waterlogging conditions. Control plants (A), inoculated plants with waterlogging (B), inoculated plants without waterlogging (C), inoculated plants with waterlogging and botanicals extracts application (D), inoculated plants with waterlogging and salicylic acid application (E), and inoculated plants with waterlogging and brassinosteroids application (F).
Citation: HortScience horts 55, 1; 10.21273/HORTSCI14550-19
The highest AUDPC values were obtained in inoculated plants with and without waterlogging, and with no synthetic elicitor sprays (80.13 and 76.36, respectively) at the end of the experiment (51 DAI), which may show a higher vascular wilt progress (Table 1; Fig. 1B and C). An intermediate development of the disease was observed in plants with Foph, under waterlogging, and sprayed with BE (68.15), whereas plants with exogenous SA (52.93) and BR (45.73) applications showed the lowest levels of the disease (Table 1; Fig. 1D–F). Trends similar to those obtained in the AUDPC were observed on the vascular wilt index (Table 1).
Area under the disease progress curve (AUDPC) and severity index of vascular wilt caused by Fusarium oxysporum f. sp. physali (Foph) in cape gooseberry plants under conditions of hypoxia in the soil and sprayed with synthetic elicitors [brassinosteroids (BR), salicylic acid (SA), or botanical extracts (BE) of Echinacea purpurea, Potentilla erecta, and Aloe vera] at 51 d after inoculation.
gS and Ψwf.
Differences were also found on gS in the interaction between Foph inoculation and synthetic elicitors at 11 (P = 0.0002) and 51 DAI (P = 0.0000) in plants under waterlogging conditions. In general, Foph presence caused a greater gS reduction in both sampling points. At 11 DAI, foliar sprays, mainly with BR or SA, obtained the highest gS values (208.9 and 194.3 mmol·m−2·s−1, respectively) under waterlogging conditions in nondiseased plants. On the other hand, it was observed that SA sprays favored a higher gS (116.8 mmol·m−2·s−1) only in Foph-inoculated cape gooseberry plants and subjected to hypoxia in the soil (Fig. 2A). At 51 DAI, the plants without pathogen presence continued recording the highest gS values. In these plants, foliar BR sprays increased this variable under oxygen deficit in the soil (241.7 mmol·m−2·s−1). A positive effect on gS was evidenced when the inoculated plants were treated with BR, SA, or BE (≈132.9 mmol·m−2·s−1) compared with diseased plants, with no synthetic elicitor sprays and under waterlogging conditions (79.2 mmol·m−2·s−1) (Fig. 2B). Differences between the evaluated factors (presence of the pathogen and synthetic elicitors) were also recorded on Ψwf at 11 and 51 DAI (P = 0.0328 and 0.0000, respectively) in waterlogged cape gooseberry plants. Foph presence in waterlogged cape gooseberry plants generated more negative Ψwf values at both sampling moments. At 11 DAI, SA or BR sprays favored the water status of noninoculated plants through a higher Ψwf under hypoxia conditions (≈−0.53 Mpa) (Fig. 2C).
Effect of synthetic elicitor [brassinosteroids (BR), salicylic acid (SA), or botanical extracts (BE) of Echinacea purpurea, Potentilla erecta, and Aloe vera] sprays on the stomatal conductance (gS) and water potential (Ψwf) of cape gooseberry plants at 11 (A, C) and 51 (B, D) days after inoculation (DAI) with (gray bars) and without (white bars) Fusarium oxysporum f. sp. physali (Foph) subjected to a short waterlogging period (6 d). Data represent the average of five plants ±se per treatment (n = 5). Bars followed by different letters indicate statistically significant differences according to the Tukey test (P ≤ 0.05).
Citation: HortScience horts 55, 1; 10.21273/HORTSCI14550-19
On the other hand, foliar BR, SA, or BE sprays had a positive effect on Ψwf (≈−0.74 Mpa) in Foph-inoculated cape gooseberry plants and subjected to hypoxia conditions in the soil (Fig. 2C). At 51 DAI, noninoculated plants and with BR sprays showed a slight increase in Ψwf values (−0.22 Mpa) under waterlogging conditions. Likewise, foliar BR, SA, or BE sprays under oxygen deficiency in the soil caused an increase of Ψwf in Foph-inoculated plants (≈−0.48 Mpa) compared with diseased and untreated plants (−0.71 Mpa) (Fig. 2D).
Plant growth variables.
Growth parameters (LA, TDW, and stem diameter) of cape gooseberry plants subjected to hypoxia showed differences (P = 0.0002, 0.0000, and 0.0164, respectively) in the interaction between Foph presence and synthetic elicitors at 51 DAI. In general, the group of plants without Foph showed the highest growth parameters compared with inoculated plants under waterlogging conditions (Fig. 3). Foliar BR, SA, or BE sprays favored LA in Foph-inoculated plants (BR 260.1 cm2, SA 238.8 cm2, and BE 204.4 cm2) under waterlogging conditions. In addition, foliar BR and SA sprays enhanced the same variable in noninoculated (BR 413.2 cm2 and SA 373.3 cm2) plants under soil oxygen deficiency (Fig. 3A). The TDW of cape gooseberry plants subjected to hypoxia in the soil was mainly favored in the treatment with BR sprays in both situations of pathogen inoculation (with and without Foph) (4.93 and 6.52 g, respectively). However, SA and BE favored this variable in inoculated cape gooseberry plants under hypoxia (Fig. 3B). Finally, foliar BR, SA, or BE sprays also produced an increase in stem diameter values in plants with and without Foph presence under the condition of oxygen deficit in the soil (Fig. 3C).
Effect of synthetic elicitor [brassinosteroids (BR), salicylic acid (SA), or botanical extracts (BE) of Echinacea purpurea, Potentilla erecta, and Aloe vera] sprays on leaf area (LA) (A), total dry weight (TDW) (B), and stem diameter (SD) (C) of cape gooseberry plants with (gray bars) and without (white bars) Fusarium oxysporum f. sp. physali (Foph) subjected to a short waterlogging period (6 d) at 51 d after inoculation (DAI). Data represent the average of five plants ±se per treatment (n = 5). Bars followed by different letters indicate statistically significant differences according to the Tukey test (P ≤ 0.05).
Citation: HortScience horts 55, 1; 10.21273/HORTSCI14550-19
Chlorophyll a fluorescence parameters.
Significant differences were observed between Foph inoculation and synthetic elicitor sprays on the chlorophyll a fluorescence parameters (Fv/Fm, ETR, qP, and NPQ) of cape gooseberry plants under waterlogging conditions at 51 DAI. Foph inoculation caused lower values of the Fv/Fm ratio, ETR, and qP of cape gooseberry plants under waterlogging conditions; however, an opposite trend was obtained with NPQ for these same plants (Fig. 4). BR, SA, or BE sprays showed two effects on the fluorescence parameters in cape gooseberry plants with waterlogging and without Foph. In the first case, the use of synthetic elicitors did not cause any differences on Fv/Fm and qP (Fig. 4A and C); in the second case, the application of these elicitors generated higher ETR (≈10.9) and lower NPQ (≈1.38) values (Fig. 4B and D). On the other hand, Foph-inoculated plants under waterlogging showed an increase in the parameters Fv/Fm (≈0.62), ETR (≈7.71), and qP (≈0.47) after the foliar treatment with BR, SA, or BE compared with inoculated plants subjected to waterlogging and without any elicitor application (0.37, 5.87, and 0.27 for Fv/Fm, ETR, and qP, respectively) (Fig. 4A–C). In contrast, a decrease in NPQ values was registered with the use of synthetic elicitors (≈1.58) compared with diseased, waterlogged, and untreated plants (2.03) (Fig. 4D).
Effect of synthetic elicitor [brassinosteroids (BR), salicylic acid (SA), or botanical extracts (BE) of Echinacea purpurea, Potentilla erecta, and Aloe vera] sprays on maximum photochemical efficiency of PSII (Fv/Fm) (A), electron transport rate (ETR) (B), photochemical quenching (qP) (C), and nonphotochemical quenching (NPQ) (D) of cape gooseberry plants with (gray bars) and without (white bars) Fusarium oxysporum f. sp. physali (Foph) subjected to a short waterlogging period (6 d) at 51 d after inoculation (DAI). Data represent the average of five plants ±se per treatment (n = 5). Bars followed by different letters indicate statistically significant differences according to the Tukey test (P ≤ 0.05).
Citation: HortScience horts 55, 1; 10.21273/HORTSCI14550-19
Leaf photosynthetic pigments.
Figure 5 shows the content of leaf photosynthetic pigments (TChl and Cx+c). Differences (P = 0.0000) were found in the photosynthetic pigment content between the evaluated factors (Foph presence × synthetic elicitors) at the end of the experiment (51 DAI). In general, the content of TChl and Cx+c was lower in Foph-inoculated plants compared with noninoculated plants under waterlogging conditions. BR, SA, or EB sprays generated an increase in the photosynthetic pigment concentration (TChl and Cx+c) in cape gooseberry plants subjected to a waterlogging period for both inoculation conditions (with and without Foph) (Fig. 5A and B).
Effect of synthetic elicitor [brassinosteroids (BR), salicylic acid (SA), or botanical extracts (BE) of Echinacea purpurea, Potentilla erecta, and Aloe vera] sprays on total chlorophyll content (TChl) (A), carotenoids (Cx+c) (B), malondialdehyde production (MDA) (C), and leaf proline content (D) of cape gooseberry plants with (gray bars) and without (white bars) Fusarium oxysporum f. sp. physali (Foph) subjected to a short waterlogging period (6 d) at 51 d after inoculation (DAI). Data represent the average of five plants ±se per treatment (n = 5). Bars followed by different letters indicate statistically significant differences according to the Tukey test (P ≤ 0.05). FW = fresh weight.
Citation: HortScience horts 55, 1; 10.21273/HORTSCI14550-19
MDA production and leaf proline content.
Significant differences were observed between Foph inoculation and synthetic elicitor sprays on MDA production (P = 0.0000) and leaf proline content (P = 0.0008) of cape gooseberry plants under waterlogging conditions at 51 DAI. Regarding these biochemical variables, opposite effects were observed in waterlogged cape gooseberry plants under both inoculation conditions (with and without Foph). A reduction of lipid peroxidation (MDA) was obtained with the application of elicitors (BR, SA, or BE), whereas a higher proline production was recorded under the foliar sprays of these inducers (Fig. 5C and D).
Biplot analysis of physiological and biochemical responses to Foph management with synthetic elicitors under waterlogging conditions.
The principal component analysis showed that the evaluated variables explained 96.6% of the physiological response of cape gooseberry plants infected with Foph, subjected to waterlogging, and treated with synthetic elicitors at 51 DAI. Figure 6A shows the evaluated variables represented by vectors and the plants of the different treatments identified with points. The vectors generated for the variables gS, Ψwf, TDW, LA, stem diameter, Fv/Fm, ETR, qP, TChl, Cx+c, and proline present angles close to the origin, showing that there is a high correlation between these variables and the plant physiological behavior. It was observed that Foph-inoculated plants without the application of elicitors under waterlogging conditions (plants + Foph + W) form a single group (I). It can be inferred that this group presented the greatest effects due to the evaluated interaction of biotic and abiotic stresses. In contrast, noninoculated plants, subjected to a short waterlogging period (6 d) and with and without BR, SA, or BE sprays (group III), were located in the sector opposite to group I, observing a positive effect of the treatments on plant physiology. On the other hand, plants with Foph under waterlogging and sprayed with the synthetic elicitors (BR, SA, or BE) showed an intermediate behavior (group II), evidencing a positive effect of the treatments with elicitors on the mitigation of the interaction between the two stresses (Foph + waterlogging). This analysis is corroborated by the cluster analysis, with the dendrogram reflecting a lower Euclidean distance between waterlogged plants with and without Foph inoculation and synthetic elicitor sprays (BR, SA, or BE). This group of plants is notably farther from the plants inoculated with the pathogen and without synthetic elicitor sprays under waterlogging conditions (Fig. 6B).
Effect of the interaction between Fusarium oxysporum f. sp. physali (Foph) inoculation and synthetic elicitor [brassinosteroids (BR), salicylic acid (SA), or botanical extracts (BE) of Echinacea purpurea, Potentilla erecta, and Aloe vera] sprays on the biplot analysis (A) and dendogram using Euclidean distance (B) of cape gooseberry plants subjected to a short waterlogging period (6 d) at 51 d after inoculation (DAI). TA = noninoculated plants without any synthetic elicitor spray; TP = Foph-inoculated plants without any synthetic elicitor spray; An = plants subjected to a short waterlogging period (6 d); BR = plants with three foliar brassinosteroid applications; SA = plants with three foliar salicylic acid applications; BE = plants with three foliar botanical extract applications; DWT = dry weight total; LA = leaf area; SD = stem diameter; Pr = proline; TChl = total chlorophyll; Cx = carotenoids; MDA = malondialdehyde; qP = photochemical quenching; NPQ = nonphotochemical quenching; Fv/Fm = photochemical efficiency of PSII; ETR = electron transport rate; gS = stomatal conductance; Ψwf = leaf water potential; PC = principal component.
Citation: HortScience horts 55, 1; 10.21273/HORTSCI14550-19
Comparative analysis of vascular wilt and waterlogging mitigation by synthetic elicitor sprays.
Table 2 shows the effect of foliar BR, SA, or BE sprays on Foph-inoculated cape gooseberry plants under waterlogging conditions (plants + W + Foph), Foph-inoculated plants without the waterlogging condition (plants + Foph), plants without Foph inoculation under waterlogging conditions (plants + W), and noninoculated plants without waterlogging and without elicitor sprays (plants without stress) at 51 DAI. These results demonstrated that three foliar BR, SA, or BE sprays helped plants to cope with the combined condition of vascular wilt and waterlogging, because a positive stimulus of these elicitors was observed on physiological and biochemical variables, such as gS, Ψwf, TDW, LA, TChl, Cx+c, Fv/Fm, ETR, MDA, and proline. In addition, the RTI based on the TDW corroborated that the foliar applications with BR, SA, or BE help to tolerate the double-stress condition in cape gooseberry plants, observing an RTI between 61.3% and 71.4% compared with the RTI of 51.3% observed in plants subjected to the two stress conditions (Foph and waterlogging) (Fig. 7).
Comparative analysis of vascular wilt and hypoxia in the soil mitigation in cape gooseberry plants by synthetic elicitor [brassinosteroids (BR), salicylic acid (SA), or botanical extracts (BE) of Echinacea purpurea, Potentilla erecta, and Aloe vera] sprays on stomatal conductance (gS), leaf water potential (Ψwf), total dry weight (TDW), leaf area (LA), stem diameter (SD), total chlorophyll (TChl), carotenoids (Cx+c), maximum PSII efficiency (Fv/Fm), electron transport rate (ETR), MDA production, and leaf proline content at 51 d after inoculation (DAI).
Effect of synthetic elicitor [brassinosteroids (BR), salicylic acid (SA), or botanical extracts (BE) of Echinacea purpurea, Potentilla erecta, and Aloe vera] sprays on the relative tolerance index (RTI) of cape gooseberry plants with and without Fusarium oxysporum f. sp. physali (Foph) subjected to a short period of waterlogging (W) (6 d) at 51 d after inoculation (DAI). Data represent the average of five plants ±se per treatment (n = 5). Bars followed by different letters indicate statistically significant differences according to the Tukey test (P ≤ 0.05).
Citation: HortScience horts 55, 1; 10.21273/HORTSCI14550-19
Discussion
The results obtained in this research confirmed previous observations in which BR, SA, or BE reduces Foph severity under oxygen deficit in the soil. BR, SA, or BE caused a decrease in the development of vascular wilt caused by F. oxysporum, which also has been documented in cucumber, tomato, and pepper, respectively (Ding et al., 2009b; Poussio et al., 2018; Yousif, 2018). BR decreases vascular wilt severity because it can participate in several physiological processes that activate the defense system (Anwar et al., 2018; Peres et al., 2019). This synthetic elicitor can also be involved in the expression of pathogenesis-related proteins, which lead to an increase in the resistance to pathogens (Ding et al., 2009b; Filek et al., 2018; Saini et al., 2015). In addition, SA can contribute to the regulation of defense against biotrophic and hemibiotrophic pathogens; it plays a key role in the systemic acquired resistance of plants, the modulation of the hypersensitivity response associated with programmed cell death, the increase in the levels of reactive oxygen species, and the activation of lipid peroxidation (Bernsdorff et al., 2016; Dempsey and Klessig, 2017; Qi et al., 2018). Finally, different BEs are constituted by aromatic hydrocarbons, such as phenylpropanoids, which are involved in various disease-resistance responses through secondary metabolite synthesis (Li et al., 2017). In this sense, commercial products based on different BEs also are rich in polysaccharides and amino acids that can induce plant defense (Jayaraman et al., 2011; Shifa et al., 2018).
Foliar synthetic elicitors sprays favored physiological and biochemical parameters, especially in cape gooseberry plants affected by hypoxia conditions in the soil. In the present study, three foliar BR, SA, or BE sprays had a positive effect mainly on the variables gS, Ψwf, growth, photosynthetic pigments, MDA, and proline. It has been reported that exogenous BR sprays at low concentrations (1 mg·L−1) can help the osmotic adjustment and induce stomatal opening. These responses improve leaf gas exchange properties, plant water status, photosynthetic pigment contents, and photochemical activity of PSII, which favor plant growth under waterlogging stress conditions (Kang et al., 2017; Li et al., 2015a; Lima and Lobato, 2017; Xia et al., 2014). Likewise, the positive effects of SA on the physiological behavior of plants under waterlogging stress conditions may be because this hormone plays an important role in the leaf’s stomatal opening and closing, the synthesis of photosynthetic pigments, the stability of membrane integrity, and the increase in the activity of antioxidant enzymes (Bai et al., 2009; Hara et al., 2012; Singh et al., 2017). Finally, BE can help to modulate the metabolism of phytohormones such as SA or jasmonic acid, and improve water and nutrient uptake, the activity of antioxidant enzymes, photosynthesis, gene expression, gS, dry matter distribution, and water relations in plants subjected to abiotic stress (Bogatek and Gniazdowska, 2007; Farooq et al., 2017; Jabran and Farooq, 2013).
Abiotic stress can negatively or positively influence the development of a disease depending on the type of pathogen, the time of infection, and the intensity of the abiotic stress (Chojak- Koźniewska et al., 2018; Pandey et al., 2017; Suzuki et al., 2014). Similarly, the use of synthetic elicitors can help the plant to stimulate physiological responses that mitigate the negative effects of both abiotic and biotic stress conditions (Naik and Al-Khayri, 2016; Thakur and Sohal, 2013). In the present study, foliar BR, SA, or BE sprays showed interesting results on the tolerance of cape gooseberry plants to conditions of combined stresses (Foph + waterlogging). Xia et al. (2009) observed that exogenous BR applications generated tolerance to the combination of cold stress and infection of cucumber mosaic virus in cucumber (Cucumis sativus L.). This tolerance was achieved through the transcriptional induction of genes involved in defense, the increase of chlorophyll fluorescence parameters (Fv/Fm and ETR) and the activity of antioxidant enzymes. Under stress conditions, BR can regulate physiological processes, such as the reduction of electrolyte leakage and MDA content. Furthermore, this synthetic elicitor also can increase proline accumulation, soluble sugars, total phenolic and glutathione contents, and antioxidant machinery activation (Anwar et al., 2018; Nawaz et al., 2017; Vardhini and Anjum, 2015). The preceding explains the positive effect of BR, which is superior at conferring tolerance to the two stress conditions (Foph and waterlogging) compared with the other elicitors evaluated in cape gooseberry plants.
SA is a plant hormone that is involved in the activation of plant defense responses against a wide range of abiotic and biotic stresses (Cekic, 2017; Fragnière et al., 2011; Hernández-Ruiz and Arnao, 2018). Studies by Mann et al. (2011) showed that foliar SA applications mitigated the negative effect of the combination of thermal stress and Huanglongbing presence in citrus fruits (Citrus sinensis L.). The evaluated variables (gS, Ψwf, growth, fluorescence parameters, MDA, and proline content) were favored after SA sprays in cape gooseberry plants under the combined stress condition (Foph and waterlogging) in the present experiment. This may be because SA is related to the activation of cell division in the meristems and the improvement of the photosynthetic rate, carboxylase activity of the Rubisco enzyme, and membrane stability. In addition, this synthetic elicitor also increases phenols, chlorophyll, carbohydrates, and proline contents, and promotes the activity of antioxidant enzymes (Asgharei, 2015; Hayat et al., 2010; Khoshbakht and Su et al., 2018).
The use of BE can be considered a promising strategy to help the plant under conditions of abiotic and biotic stress (Ben Salah et al., 2018; Santaniello et al., 2017; Shukla et al., 2017). Maymoune et al. (2015) observed that the application of BE of green algae (Ulva sp.) decreased the necrosis diameter, inhibited spore germination, and increased protection efficacy in tomato plants (Solanum lycopersicum L.) infected with Botrytis cinerea under water stress conditions. Although BR and SA sprays showed better results than those obtained with BE from plants of E. purpurea, P. erecta, and A. vera, these extracts also favored the physiological response of Foph-inoculated cape gooseberry plants under hypoxia conditions in the soil. This positive effect of BE can be because these compounds stimulate plant growth and development, improve water and nutrient uptake efficiency, regulate stomatal dynamics, and increase the ascorbate content and the antioxidant enzyme activity (Carvalho et al., 2018; Guinan et al., 2012; Howladar, 2014; Shukla et al., 2017).
Conclusion
This study showed that sprays of synthetic elicitors, such as BR, SA, or BE, reduced vascular wilt severity by improving the physiological and biochemical response of Foph-infected cape gooseberry plants under hypoxia conditions in the soil. Likewise, it was observed that the use of these elicitors has positive effects on plant physiology, favoring gS, Ψwf, growth (expressed as dry matter accumulation and LA), photochemical efficiency of PSII, ETR, qP, TChl, and proline content. Synthetic elicitor sprays also showed a significant reduction of NPQ and lipid peroxidation of membranes under a combination of stress conditions (Foph + waterlogging); however, additional research is needed on topics such as gene expression as a product of these synthetic elicitor sprays. In addition, field trials are suggested to evaluate the effect of BR, SA, or BE on crop yield and fruit quality parameters under the interaction of these two stresses (Foph and waterlogging). The obtained results suggest that BR, SA, or EB sprays in cape gooseberry plants could be considered as an alternative for the integrated management of vascular wilt in cape gooseberry–producing areas where waterlogging episodes could be expected.
Literature Cited
Abdallah, R.A.B., Jabnoun-Khiareddine, H., Nefzi, A., Mokni-Tlili, S. & Daami-Remadi, M. 2016 Biocontrol of fusarium wilt and growth promotion of tomato plants using endophytic bacteria isolated from Solanum elaeagnifolium stems J. Phytopathol. 164 10 121 132
Agronet 2019 Área, Producción y Rendimiento Nacional de uchuva en Colombia. Red de información y comunicación del sector agropecuario. 20 May 2019. <www.agronet.gov.co/estadistica/Paginas/home.aspx?cod=1#>
Aguilar, E.A., Turner, D.W. & Sivasithamparam, K. 2000 Fusarium oxysporum f. sp. cubense inoculation and hypoxia alter peroxidase and phenylalanine ammonia lyase activities in nodal roots of banana cultivars (Musa sp.) differing in their susceptibility to Fusarium wilt Aust. J. Bot. 48 5 121 132
Aldana, F., García, P.N. & Fischer, G. 2014 Effect of waterlogging stress on the growth, development and symptomatology of cape gooseberry (Physalis peruviana L.) plants Rev. Acad. Colomb. Cienc. Exactas Fis. Nat. 38 14 121 132
Álvarez-Flórez, F., López-Cristoffanini, C., Jáuregui, O., Melgarejo, L.M. & López-Carbonell, M. 2017 Changes in ABA, IAA and JA levels during calyx, fruit and leaves development in cape gooseberry plants (Physalis peruviana L.) Plant Physiol. Biochem. 115 174 182
Alves, D.P., Tomaz, R.S., Laurindo, B.S., Laurindo, R.D.F., Cruz, C.D., Nick, C. & Silva, D.J.H.D. 2017 Artificial neural network for prediction of the area under the disease progress curve of tomato late blight Sci. Agr. 74 1 121 132
Anwar, A., Liu, Y., Dong, R., Bai, L., Yu, X. & Li, Y. 2018 The physiological and molecular mechanism of brassinosteroid in response to stress: A review Biol. Res. 51 46
Bai, T., Li, C., Ma, F., Shu, H. & Han, M. 2009 Exogenous salicylic acid alleviates growth inhibition and oxidative stress induced by hypoxia stress in Malus robusta Rehd J. Plant Growth Regul. 28 4 121 132
Bates, L.S., Waldren, R.P. & Teare, I.D. 1973 Rapid determination of free proline for water-stress studies Plant Soil 39 1 121 132
Bektas, Y. & Eulgem, T. 2015 Synthetic plant defense elicitors Front. Plant Sci. 5 804
Ben Salah, I., Aghrouss, S., Douira, A., Aissam, S., El Alaoui-Talibi, Z., Filali-Maltouf, A. & El Modafar, C. 2018 Seaweed polysaccharides as bio-elicitors of natural defenses in olive trees against verticillium wilt of olive J. Plant Interact. 13 1 121 132
Bernal-Vicente, A., Petri, C., Hernandez, J.A. & Diaz-Vivancos, P. 2017 The effect of abiotic and biotic stress on the salicylic acid biosynthetic pathway from mandelonitrile in peach bioRxiv 204636
Bernsdorff, F., Döring, A.C., Gruner, K., Schuck, S., Bräutigam, A. & Zeier, J. 2016 Pipecolic acid orchestrates plant systemic acquired resistance and defense priming via salicylic acid-dependent and - independent pathways Plant Cell 28 102 129
Bibi, N., Fan, K., Dawood, M., Nawaz, G., Yuan, S. & Xuede, W. 2014 Exogenous application of epibrassinolide attenuated Verticillium wilt in upland cotton by modulating the carbohydrates metabolism, plasma membrane ATPases and intracellular osmolytes Plant Growth Regulat. 73 2 121 132
Bogatek, R. & Gniazdowska, A. 2007 ROS and phytohormons in plant-plant allelopathic interaction Plant Signal. Behav. 2 4 121 132
Campbell, C.L. & Madden, L.V. 1990 Introduction to plant disease epidemiology. First ed. Wiley-Interscience, New York
Carvalho, M.E.A., de Camargo, P.R., Gaziola, S.A. & Azevedo, R.A. 2018 Is seaweed extract an elicitor compound? Changing proline content in drought-stressed bean plants Comun. Sci. 9 2 121 132
Cekic, F.O. 2017 Effects of salicylic acid on gaba metabolism in pepper plants under stress conditions Hacet. J. Biol. Chem. 45 3 121 132
Chávez-Arias, C.C., Gómez-Caro, S. & Restrepo-Díaz, H. 2019 Physiological, biochemical and chlorophyll fluorescence parameters of Physalis Peruviana L. seedlings exposed to different short-term waterlogging periods and fusarium wilt infection Agronomy 9 5 213
Chiang, K.S., Liu, H.I. & Bock, C.H. 2017 A discussion on disease severity index values. Part I: Warning on inherent errors and suggestions to maximise accuracy Ann. Appl. Biol. 171 2 121 132
Chojak-Koźniewska, J., Kuźniak, E. & Zimny, J. 2018 The effects of combined abiotic and pathogen stress in plants: Insights from salinity and Pseudomonas syringae pv lachrymans interaction in cucumber Front. Plant Sci. 9 1691
Csiszár, J., Brunner, S., Horváth, E., Bela, K., Ködmön, P., Riyazuddin, R., Gallé, Á., Hurton, Á., Papdi, C., Szabados, L. & Tari, I. 2018 Exogenously applied salicylic acid maintains redox homeostasis in salt-stressed Arabidopsis gr1 mutants expressing cytosolic roGFP1 Plant Growth Regulat. 86 2 121 132
Dar, M.I., Naikoo, M.I., Rehman, F., Naushin, F. & Khan, F.A. 2016 Proline accumulation in plants: Roles in stress tolerance and plant development, p. 155–166. In: N. Iqbal, R. Nazar, and N.A. Khan (eds.). Osmolytes and plants acclimation to changing environment: Emerging omics technologies. Springer, New Delhi, India
Dempsey, D.A. & Klessig, D.F. 2017 How does the multifaceted plant hormone salicylic acid combat disease in plants and are similar mechanisms utilized in humans? BMC Biol. 15 23
Ding, J., Shi, K., Zhou, Y.H. & Yu, J.Q. 2009a Effects of root and foliar applications of 24-epibrassinolide on Fusarium wilt and antioxidant metabolism in cucumber roots HortScience 44 1340 1345
Ding, J., Shi, K., Zhou, Y.H. & Yu, J.Q. 2009b Microbial community responses associated with the development of Fusarium oxysporum f. sp. cucumerinum after 24-epibrassinolide applications to shoots and roots in cucumber Eur. J. Plant Pathol. 124 1 121 132
Duncan, J.M. & Kennedy, D.M. 1989 The effect of waterlogging on Phytophthora root rot of red raspberry Plant Pathol. 38 2 121 132
Dutta Gupta, S., Auge, R.M., Denchev, P.D. & Conger, B.V. 1995 Growth, proline accumulation and water relations in NaCl-selected and non-selected callus lines of Dactylis glomerata Environ. Expt. Bot. 35 1 121 132
Elansary, H.O., Yessoufou, K., Abdel-Hamid, A.M., El-Esawi, M.A., Ali, H.M. & Elshikh, M.S. 2017 Seaweed extracts enhance Salam turfgrass performance during prolonged irrigation intervals and saline shock Front. Plant Sci. 8 830
Fariduddin, Q., Yusuf, M., Ahmad, I. & Ahmad, A. 2014 Brassinosteroids and their role in response of plants to abiotic stresses Biol. Plant. 58 1 121 132
Farooq, M., Rizwan, M., Nawaz, A., Rehman, A. & Ahmad, R. 2017 Application of natural plant extracts improves the tolerance against combined terminal heat and drought stresses in bread wheat J. Agron. Crop Sci. 203 6 121 132
Filek, M., Sieprawska, A., Oklestkova, J., Rudolphi-Skórska, E., Biesaga-Kościelniak, J., Miszalski, Z. & Janeczko, A. 2018 24-Epibrassinolide as a modifier of antioxidant activities and membrane properties of wheat cells in zearalenone stress conditions J. Plant Growth Regul. 37 4 121 132
Fragnière, C., Serrano, M., Abou-Mansour, E., Métraux, J.P. & L’haridon, F. 2011 Salicylic acid and its location in response to biotic and abiotic stress FEBS Lett. 585 12 121 132
Groves, E., Howard, K., Hardy, G. & Burgess, T. 2015 Role of salicylic acid in phosphite-induced protection against Oomycetes; a Phytophthora cinnamomi-Lupinus augustifolius model system Eur. J. Plant Pathol. 141 3 121 132
Guinan, K.J., Sujeeth, N., Copeland, R.B., Jones, P.W., O’brien, N.M., Sharma, H.S.S., Prouteau, P.F.J. & O’Sullivan, J.T. 2012 Discrete roles for extracts of Ascophyllum nodosum in enhancing plant growth and tolerance to abiotic and biotic stresses Acta Hort. 1009 127 135
Hainaut, P., Remacle, T., Decamps, C., Lambert, R. & Sadok, W. 2016 Higher forage yields under temperate drought explained by lower transpiration rates under increasing evaporative demand Eur. J. Agron. 72 91 98
Hara, M., Furukawa, J., Sato, A., Mizoguchi, T. & Miura, K. 2012 Abiotic stress and role of salicylic acid in plants, p. 235–251. In: P. Ahmad and M.N.V. Prasad (eds.). Abiotic stress responses in plants. Springer, New York
Hayat, Q., Hayat, S., Irfan, M. & Ahmad, A. 2010 Effect of exogenous salicylic acid under changing environment: A review Environ. Expt. Bot. 68 1 121 132
He, L., Yu, L., Li, B., Du, N. & Guo, S. 2018 The effect of exogenous calcium on cucumber fruit quality, photosynthesis, chlorophyll fluorescence, and fast chlorophyll fluorescence during the fruiting period under hypoxic stress BMC Plant Biol. 18 180
Hernández-Ruiz, J. & Arnao, M. 2018 Relationship of melatonin and salicylic acid in biotic/abiotic plant stress responses Agronomy 8 4 33
Herzog, M., Striker, G.G., Colmer, T.D. & Pedersen, O. 2016 Mechanisms of waterlogging tolerance in wheat–a review of root and shoot physiology Plant Cell Environ. 39 5 121 132
Hodges, D.M., DeLong, J.M., Forney, C.F. & Prange, R.K. 1999 Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds Planta 207 4 121 132
Howladar, S.M. 2014 A novel Moringa oleifera leaf extract can mitigate the stress effects of salinity and cadmium in bean (Phaseolus vulgaris L.) plants Ecotoxicol. Environ. Saf. 100 69 75
Irulappan, V. & Senthil-Kumar, M. 2018 Morpho-physiological traits and molecular intricacies associated with tolerance to combined drought and pathogen stress in plants, p. 59–74. In: S.S. Gosal and S.H. Wani (eds.). Biotechnologies of crop improvement. Springer, Cham, Switzerland
Jabran, K. & Farooq, M. 2013 Implications of potential allelopathic crops in agricultural systems, p. 349–385. In: Z.A. Cheema, M. Farooq, and A. Wahid (eds.). Allelopathy current trends and future applications. Springer, Berlin, Germany
Jayaraman, J., Norrie, J. & Punja, Z.K. 2011 Commercial extract from the brown seaweed Ascophyllum nodosum reduces fungal diseases in greenhouse cucumber J. Appl. Phycol. 23 3 121 132
Joseph, A., Ese, E.A., Ademiluyi, B.O. & Aluko, P.A. 2017 Efficacy of selected plant extracts in the management of tomato early blight disease caused by Alternaria solani Asian J. Plant Pathol. 11 1 121 132
Kang, Y.H., Breda, A. & Hardtke, C.S. 2017 Brassinosteroid signaling directs formative cell divisions and protophloem differentiation in Arabidopsis root meristems Development 144 272 280
Khan, M.I.R., Fatma, M., Per, T.S., Anjum, N.A. & Khan, N.A. 2015 Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants Front. Plant Sci. 6 462
Khoshbakht, D. & Asgharei, M.R. 2015 Influence of foliar-applied salicylic acid on growth, gas-exchange characteristics, and chlorophyll fluorescence in citrus under saline conditions Photosynthetica 53 3 121 132
Król, P., Igielski, R., Pollmann, S. & Kępczyńska, E. 2015 Priming of seeds with methyl jasmonate induced resistance to hemi-biotroph Fusarium oxysporum f. sp. lycopersici in tomato via 12-oxo-phytodienoic acid, salicylic acid, and flavonol accumulation J. Plant Physiol. 179 122 132
Leslie, J.F. & Summerell, B.A. 2006 The Fusarium laboratory manual. 1st ed. Blackwell Publishing, Ames, IA
Li, J., Yang, P., Gan, Y., Yu, J. & Xie, J. 2015a Brassinosteroid alleviates chilling-induced oxidative stress in pepper by enhancing antioxidation systems and maintenance of photosystem II Acta Physiol. Plant. 37 222
Li, Y.P., You, M.P., Colmer, T.D. & Barbetti, M.J. 2015b Effect of timing and duration of soil saturation on soilborne Pythium diseases of common bean (Phaseolus vulgaris) Plant Dis. 99 1 121 132
Li, G., Zhu, S., Wu, W., Zhang, C., Peng, Y., Wang, Q. & Shi, J. 2017 Exogenous nitric oxide induces disease resistance against Monilinia fructicola through activating the phenylpropanoid pathway in peach fruit J. Sci. Food Agr. 97 9 121 132
Lima, J.V. & Lobato, A.K.S. 2017 Brassinosteroids improve photosystem II efficiency, gas exchange, antioxidant enzymes and growth of cowpea plants exposed to water deficit Physiol. Mol. Biol. Plants 23 1 121 132
Liu, Z., Cheng, R., Xiao, W., Guo, Q. & Wang, N. 2014 Effect of off-season flooding on growth, photosynthesis, carbohydrate partitioning, and nutrient uptake in Distylium chinense PLoS One 9 9 e107636
Llorens, E., García-Agustín, P. & Lapeña, L. 2017 Advances in induced resistance by natural compounds: Towards new options for woody crop protection Sci. Agr. 74 1 121 132
Mandal, S., Mallick, N. & Mitra, A. 2009 Salicylic acid-induced resistance to Fusarium oxysporum f. sp. lycopersici in tomato Plant Physiol. Biochem. 47 7 121 132
Mann, K.K., Schumann, A.W. & Spann, T.M. 2011 Response of citrus to exogenously applied salicylate compounds during abiotic and biotic stress Proc. Annu. Meet. Fla. State Hort. Soc. 124 101 110
Mansori, M., Chernane, H., Latique, S., Benaliat, A., Hsissou, D. & El Kaoua, M. 2015 Seaweed extract effect on water deficit and antioxidative mechanisms in bean plants (Phaseolus vulgaris L.) J. Appl. Phycol. 27 4 121 132
Maymoune, A., Adeline, P., Marie, T., Sophie, G., Sophie, C., Catherine, L., Claire, N. & Sonia, H. 2015 Impact of abiotic stresses on the protection efficacy of defence elicitors and on metabolic regulation in tomato leaves infected by Botrytis cinerea Eur. J. Plant Pathol. 142 2 121 132
McGovern, R.J. 2015 Management of tomato diseases caused by Fusarium oxysporum Crop Prot. 73 78 92
Moreno-Velandia, C.A. 2017 Interactions between Bacillus amyloliquefaciens Bs006, Fusarium oxysporun Map5 and Cape gooseberry (Physalis peruviana). Natl. Univ. of Colombia, Bogotá, PhD Diss
Moreno-Velandia, C.A., Izquierdo-García, L.F., Ongena, M., Kloepper, J.W. & Cotes, A.M. 2019 Soil sterilization, pathogen and antagonist concentration affect biological control of Fusarium wilt of cape gooseberry by Bacillus velezensis Bs006 Plant Soil 435 1-2 121 132
Moslemi, A., Ades, P.K., Groom, T., Nicolas, M.E. & Taylor, P.W. 2018 Influence of waterlogging on growth of pyrethrum plants infected by the crown and root rot pathogens, Fusarium oxysporum, Fusarium avenaceum and Paraphoma vinacea. Austral Plant Pathol. 47 2 121 132
Mostafa, A.A., Al-Askar, A.A., Almaary, K.S., Dawoud, T.M., Sholkamy, E.N. & Bakri, M.M. 2018 Antimicrobial activity of some plant extracts against bacterial strains causing food poisoning diseases Saudi J. Biol. Sci. 25 2 121 132
Naik, P.M. & Al-Khayri, J.M. 2016 Abiotic and biotic elicitors—role in secondary metabolites production through in vitro culture of medicinal plants, p. 247–277. In: A. Shanker and C. Shanker (eds.). Abiotic and biotic stress in plants—recent advances and future perspectives. IntechOpen, Rijeka, Croatia
Nawaz, F., Naeem, M., Zulfiqar, B., Akram, A., Ashraf, M.Y., Raheel, M., Shabbir, R.N., Hussain, R.A., Anwar, I. & Aurangzaib, M. 2017 Understanding brassinosteroid-regulated mechanisms to improve stress tolerance in plants: A critical review Environ. Sci. Pollut. Res. Int. 24 19 121 132
Olivares-Tenorio, M.L., Dekker, M., van Boekel, M.A. & Verkerk, R. 2017 Evaluating the effect of storage conditions on the shelf life of cape gooseberry (Physalis peruviana L.) Lebensm. Wiss. Technol. 80 523 530
Osorio-Guarín, J.A., Enciso-Rodríguez, F.E., González, C., Fernández-Pozo, N., Mueller, L.A. & Barrero, L.S. 2016 Association analysis for disease resistance to Fusarium oxysporum in cape gooseberry (Physalis peruviana L) BMC Genomics 17 248
Otie, V., Ping, A., Udo, I. & Eneji, E. 2019 Brassinolide effects on maize (Zea mays L.) growth and yield under waterlogged conditions J. Plant Nutr. 42 8 121 132
Pandey, P., Irulappan, V., Bagavathiannan, M.V. & Senthil-Kumar, M. 2017 Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits Front. Plant Sci. 8 537
Park, D. 1961 Isolation of Fusarium oxysporum from soils Trans. Br. Mycol. Soc. 44 1 121 132
Peres, A.L.G., Soares, J.S., Tavares, R.G., Righetto, G., Zullo, M.A., Mandava, N.B. & Menossi, M. 2019 Brassinosteroids, the sixth class of Phytohormones: A molecular view from the discovery to hormonal interactions in plant development and stress adaptation Int. J. Mol. Sci. 20 2 331
Poussio, G.B., Abro, M.A., Hajano, J.U., Khaskheli, M.I., Rajput, K.I. & Memon, S.R. 2018 Potential of plant extracts and fungicides for managing Fusarium oxysporum f. sp lycopersici Pak. J. Phytopathol. 30 1 121 132
Procolombia 2019 Uchuva (Goldenberry). Exportaciones, turismo, inversion marca país. 18 Apr. 2019. <www.procolombia.co/docs/int-procolombia/es/exportaciones/ficha_uchuva_final.pdf>
Qi, G., Chen, J., Chang, M., Chen, H., Hall, K., Korin, J., Liu, F., Wang, D. & Fu, Z.Q. 2018 Pandemonium breaks out: Disruption of salicylic acid-mediated defense by plant pathogens Mol. Plant 11 12 121 132
Ramírez-Godoy, A., Vera-Hoyos, M.P., Jiménez-Beltrán, N. & Restrepo-Diaz, H. 2018 Application of foliar synthetic elicitors for the management of Diaphorina citri (Hemiptera: Liviidae) populations in Tahiti lime (Citrus latifolia Tanaka) HortScience 53 1012 1020
Rao, X. & Dixon, R.A. 2017 Brassinosteroid mediated cell wall remodeling in grasses under abiotic stress Front. Plant Sci. 8 806
Rao, R. & Li, Y. 2003 Management of flooding effects on growth of vegetable and selected field crops HortTechnology 13 610 616
Rongai, D., Pulcini, P., Pesce, B. & Milano, F. 2017 Antifungal activity of pomegranate peel extract against fusarium wilt of tomato Eur. J. Plant Pathol. 147 1 121 132
Roussos, P.A., Denaxa, N.K., Damvakaris, T., Stournaras, V. & Argyrokastritis, I. 2010 Effect of alleviating products with different mode of action on physiology and yield of olive under drought Scientia Hort. 125 4 121 132
Saini, S., Sharma, I. & Pati, P.K. 2015 Versatile roles of brassinosteroid in plants in the context of its homoeostasis, signaling and crosstalks Front. Plant Sci. 6 950
Santaniello, A., Scartazza, A., Gresta, F., Loreti, E., Biasone, A., Di Tommaso, D., Piaggesi, A. & Perata, P. 2017 Ascophyllum nodosum seaweed extract alleviates drought stress in Arabidopsis by affecting photosynthetic performance and related gene expression Front. Plant Sci. 8 1362
Shao, G.C., Lan, J.J., Yu, S.E., Liu, N., Guo, R.Q. & She, D.L. 2013 Photosynthesis and growth of winter wheat in response to waterlogging at different growth stages Photosynthetica 51 3 121 132
Shifa, H., Gopalakrishnan, C. & Velazhahan, R. 2018 Management of late leaf spot (Phaeoisariopsis personata) and root rot (Macrophomina phaseolina) diseases of groundnut (Arachis hypogaea L.) with plant growth-promoting rhizobacteria, systemic acquired resistance inducers and plant extracts Phytoparasitica 46 1 121 132
Shivas, R.G., Wood, P.M., Darcey, M.W. & Peg, K.G. 1995 First record of Fusarium oxysporum f. sp. cubense on Cavendish bananas in Western Australia Austral. Plant Pathol. 24 1 121 132
Shukla, P.S., Shotton, K., Norman, E., Neily, W., Critchley, A.T. & Prithiviraj, B. 2017 Seaweed extract improve drought tolerance of soybean by regulating stress-response genes AoB Plants 10 1 plx051
Simbaqueba, J., Catanzariti, A.M., González, C. & Jones, D.A. 2018 Evidence for horizontal gene transfer and separation of effector recognition from effector function revealed by analysis of effector genes shared between cape gooseberry-and tomato-infecting formae speciales of Fusarium oxysporum Mol. Plant Pathol. 19 10 121 132
Sims, D.A. & Gamon, J.A. 2002 Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages Remote Sens. Environ. 81 2-3 121 132
Singh, S.K., Singh, A.K. & Dwivedi, P. 2017 Modulating effect of salicylic acid in tomato plants in response to waterlogging stress Intl. J. Agr. Environ. Biotechnol. 10 1 121 132
Su, H., Song, S., Yan, X., Fang, L., Zeng, B. & Zhu, Y. 2018 Endogenous salicylic acid shows different correlation with baicalin and baicalein in the medicinal plant Scutellaria baicalensis Georgi subjected to stress and exogenous salicylic acid PLoS One 13 2 e0192114
Suzuki, N., Rivero, R.M., Shulaev, V., Blumwald, E. & Mittler, R. 2014 Abiotic and biotic stress combinations New Phytol. 203 1 121 132
Thakur, M. & Sohal, B.S. 2013 Role of elicitors in inducing resistance in plants against pathogen infection: A review ISRN Biochem. 2013 762412
Van Oosten, M.J., Pepe, O., De Pascale, S., Silletti, S. & Maggio, A. 2017 The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants Chem. Biol. Technol. Agr. 4 5
Vardhini, B.V. & Anjum, N.A. 2015 Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system Front. Environ. Sci. 2 67
Villarreal-Navarretex, A., Fischer, G., Melgarejo, L.M., Correa, G. & Hoyos-Carvajal, L. 2017 Growth response of the cape gooseberry (Physalis peruviana L.) to waterlogging stress and Fusarium oxysporum infection Acta Hort. 1178 161 168
Wellburn, A.R. 1994 The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution J. Plant Physiol. 144 3 121 132
Wilcox, W.F. 1993 Incidence and severity of crown and root rots on four apple rootstocks following exposure to Phytophthora species and waterlogging J. Amer. Soc. Hort. Sci. 118 1 121 132
Wu, X., Tang, Y., Li, C., Wu, C. & Huang, G. 2015 Chlorophyll fluorescence and yield responses of winter wheat to waterlogging at different growth stages Plant Prod. Sci. 18 3 121 132
Xia, X.J., Wang, Y.J., Zhou, Y.H., Tao, Y., Mao, W.H., Shi, K., Asami, T., Chen, Z. & Yu, J.Q. 2009 Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber Plant Physiol. 150 801 814
Xia, X.J., Gao, C.J., Song, L.X., Zhou, Y.H., Shi, K.A.I. & Yu, J.Q. 2014 Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum Plant Cell Environ. 37 9 121 132
Xue, L.J., Guo, W., Yuan, Y., Anino, E.O., Nyamdari, B., Wilson, M.C., Frost, C.J., Chen, H.Y., Babst, B.A., Harding, S.A. & Tsai, C.J. 2013 Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state but not growth in transgenic Populus Plant Cell 25 7 121 132
Yousif, D.Y. 2018 Effects sprayed solution of salicylic acid to prevent of wilt disease caused by Fussarium oxysporium J. Phys. Conf. Ser. 1003 012001
Zhang, D.W., Deng, X.G., Fu, F.Q. & Lin, H.H. 2015 Induction of plant virus defense response by brassinosteroids and brassinosteroid signaling in Arabidopsis thaliana Planta 241 4 121 132
Zhu, M., Li, F.H. & Shi, Z.S. 2016 Morphological and photosynthetic response of waxy corn inbred line to waterlogging Photosynthetica 54 4 121 132