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Article

Plant Physiological Assessments on Promising New HLB-Tolerant Citrus Rootstocks after Inoculation with the Phytopathogenic Ascomycete Rosellinia necatrix

by
Juan M. Arjona-López
1,*,
Frederick G. Gmitter, Jr.
2,
Estefanía Romero-Rodríguez
1,
Jude W. Grosser
2,
José Luís Cantero-Sánchez
1,
Carlos J. López-Herrera
3 and
Francisco J. Arenas-Arenas
1
1
Department of Agri-Food Engineering and Technology, Andalusian Institute of Agricultural and Fisheries Research and Training (IFAPA), “Las Torres” Center, Ctra. Sevilla-Cazalla de la Sierra km. 12.2, Alcalá del Río, 41200 Seville, Spain
2
Citrus Research and Education Center, Department of Horticultural Sciences, IFAS, University of Florida, Lake Alfred, FL 33850, USA
3
Institute for Sustainable Agriculture, Spanish Research Council, Alameda del Obispo s/n, 14004 Cordoba, Spain
*
Author to whom correspondence should be addressed.
Horticulturae 2023, 9(7), 744; https://doi.org/10.3390/horticulturae9070744
Submission received: 28 April 2023 / Revised: 20 June 2023 / Accepted: 22 June 2023 / Published: 25 June 2023
(This article belongs to the Special Issue Advanced Diagnosis and Control Strategies of Plant Pests and Diseases in Horticulture)
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Abstract

:
Citriculture is considered the most important fruit industry and involves the cultivation of several fruit varieties, which are susceptible to many plant pathogens. In this sense, soil-borne pathogenic fungi, such Rosellinia necatrix, threaten citrus fruit production worldwide because they can cause fruit loss. Therefore, we assayed the physiological reaction of novel citrus rootstocks against white root rot disease during long-term management. Data from above-ground symptoms and chlorophyll content were periodically obtained during the experimental process. In addition, plant leaf area and percentage of biomass reduction were determined for each rootstock when the experiment finished. The behavior of the inoculated tolerant rootstocks was as follows: the lowest symptom rate of SAUDPC was achieved by B11R5T25 and N40R3T25; AMB+CZO manifested the highest disease incidence; B11R5T25 and A+VOLK × Orange 19-11-8 displayed the highest and the lowest chlorophyll content, respectively; AMB+CZO and A+VOLK × Orange 19-11-8 showed the highest biomass reduction, and the lowest was detected in B11R5T25 and N40R2T19; concerning the leaf area, N40R1T18, N40R3T25 and N40R2T19 showed the lowest response, and 2247 × 2075-01-2 achieved the highest rate. In summary, B11R5T25 and N40R3T25 displayed the lowest disease rate.

1. Introduction

Biotic factors such as plant pathogens are limiting agents that have reduced crop production since the beginning of agriculture. Depending on the crop type, environmental conditions and location, biotic factors and plant pathogens can cause losses ranging between 11 to 59% and 3 to 24%, respectively [1]. In this sense, Citrus (Rutaceae family) are also affected by plant pathogens causing pre-harvest diseases as well as crop losses.
Rosellinia necatrix (Prill.) is a soil-borne phytopathogenic ascomycete described in all continents except Antarctica [2]. This phytopathogen is very polyphagous due to its ability to infect more than 340 plant species [3], whereby it induces white root rot disease (WRR) and results in important economic losses, especially in woody crops as major hosts, including citrus [2,4,5,6]. Contrarily to Phytophthora citrus diseases, the control strategies for WRR are not fully effective because R. necatrix has a long latency in soil, is an extensive host species, and can tolerate many chemical compounds [2]. Some control tools developed in other crops include irrigation management [7], soil solarization [8,9,10], antagonistic fungi [8,11,12,13,14,15,16], antagonistic rhizobacteria [17,18,19], mycoviruses [20,21,22], antagonistic bacteria, antagonistic fungi plus a fungicide [23,24,25], and different synthetic fungicides as chemical controls [26,27,28,29,30]. Nevertheless, most of these chemical compounds for controlling R. necatrix are banned for agricultural use in the European Union (EU) [31], and all of them are banned in Spanish citrus orchards [32]. Additionally, EU authorities are constantly reducing the list of permitted pesticides in agriculture, as described in Directive 2009/128/CE and “farm to fork” strategy (European Green Deal), the latter of which aims to reduce 50% of hazardous pesticides by 2030 [33].
Traditionally, the cultivation of tolerant citrus rootstocks has helped to reduce the incidence of phytopathogenic diseases caused by Phytophthora spp., nematodes and citrus tristeza virus (CTV) [34]. Nevertheless, little information is available relating to citrus plant material and WRR tolerance. Two previous works assessed the incidence of R. necatrix in different rootstocks, in which P. trifoliata and two new candidates (P. trifoliata descendants) showed the highest levels of tolerance [5,35]. In the case of other fruit trees (apple, avocado, grapevine and persimmon), breeding researchers have obtained tolerant rootstocks against R. necatrix [36,37,38,39,40,41,42]. As a consequence, the use of tolerant plant material can be positioned and integrated as an optimal control strategy in woody orchards with WRR problems.
Citrus crops are notably grown in the Mediterranean and regions with subtropical climates, where they constitute one of the most relevant fruit sectors. In 2021, Spain was the fifth highest producer of total citrus crops, producing 6.7 million tons, and it was the first fresh fruit exporter, exporting 3.5 million tons worldwide [43]. The Valencian and Andalusian regions were responsible for more than 80% of the production [44]. In this country, R. necatrix is reported as an endemic phytopathogen located in different regions, including Valencia and Andalusia, and targets several fruit crops [45,46,47,48,49]. Furthermore, citrus-producing countries in the Mediterranean basin face the threat of emerging diseases, including Huanglongbing or citrus greening disease (HLB). HLB is the most destructive disease in citriculture worldwide [50], and it is caused by three species of bacteria from the genus Candidatus Liberibacter [51,52], which are vectored by psyllid insects, principally Trioza erytreae and Diaphorina citri [53,54,55,56]. To date, the non-causal agent of HLB has been reported in the Mediterranean basin region [57,58]. However, T. erytreae has been spreading along the Atlantic coastal area of Iberian mainland from the north to the south since 2014 [59,60,61], and D. citri was first found in mandarin and orange trees from Israel in 2021 [57].
Currently, the main breeding programs from around the world have incorporated, among others, conventional biotic stresses (Phytophthora, nematodes or CTV) into the evaluation of new citrus rootstocks facing HLB [34,62], but R. necatrix disease has not been considered. Therefore, the purpose of this research was to determine the susceptibility of novel HLB-tolerant citrus rootstocks from the breeding program of the Citrus Research and Education Center (CREC), University of Florida, to WRR.

2. Materials and Methods

2.1. Plant Material and Experimental Design

In total, 198 plants from 11 different citrus rootstocks were assessed in this study. Ten of these rootstocks (5 diploids and 5 tetraploids) were recently obtained from the breeding program of CREC, whereas Carrizo citrange (diploid) was used as comparative candidate (Table 1). This rootstock was available from the Spanish office of plant varieties under the registered number 16690003 [63]. All plants were first grown from in vitro culture, cultivated in 3 litre plastic pots containing coconut fiber (80%) and peat (20%) substrate, and enriched with 5 g of Osmocote ® Pro (16 + 11 + 10 + 2 MgO + trace elements, longevity 12–14 months) per litre of substrate and supplied by Agromillora Group nursery (Subirats, Barcelona, Spain) at the age of three. When the plants were received, they were separated into two lots for each R. necatrix effect (inoculated and control (non-inoculated)) and distributed into random conditions within a greenhouse. The experiment was carried out during the spring-summer-autumn seasons of 2022 under controlled conditions (24.5 °C and relative humidity of 69.3%) in a greenhouse located in “Las Torres” Center. Each R. necatrix effect and rootstock comprised nine replicates (n = 9); thus, a total of 18 plants were used per rootstock in both R. necatrix effects.

2.2. Fungal Isolate

The fungal isolate of R. necatrix (Rn452), with high pathogenicity, was provided from the fungal collection at the Institute for Sustainable Agriculture (IAS). The species was morphologically identified by the in vitro growth of white and cottony mycelium, and the microscopic presence of pear-shaped swellings in the hypha close to the septum. Later, this visual identification was molecularly confirmed following the methodology of Arjona-López [72]. Thus, the sequence showed 100% identity to the corresponding region of R. necatrix and was uploaded to the GenBank database (accession number: OP482261).

2.3. Plant Inoculation

The plant inoculation process was performed following the methodology of Sztejnberg and Madar [5]. In brief, an R. necatrix isolate from the stock culture was cultured on 15 mL of potato dextrose agar (15 mL; PDA; Difco Laboratories, Detroit, MI, USA) on Petri plates (90 mm in diameter) for refreshing and kept for 7 days at 25 °C in darkness. Next, wheat seeds were moistened in 1000 mL Teqler flasks for one day and double-sterilized after removing the water. Thus, wheat grains were inoculated with mycelial disks of refreshed Rn452 and incubated for three weeks at 25 °C in darkness until the fungus fully colonized the grains. Finally, the plants from the Rn452 effect were ready for inoculation by depositing the inoculum in each pot next to roots at a proportion of 3.75 g of colonized wheat grains to one litre of substrate.

2.4. Evaluation of Aerial Plant Symptoms

The examination of WRR disease was carried out at the aerial part of the plants in both R. necatrix effects and rootstocks using a symptom scale of 1–5 [35] (Figure 1). Plant symptom evaluations were carried out twice per week for 269 days since the beginning of the experiment (inoculation day) until all plants from one rootstock and with the Rn452 effect died. Symptom values were used to obtain the standardized area under the disease progress curve (SAUDPC), adapted from [73,74]:
A U D P C = ∑ i − 1 n − 1 y i + y i + 1 2 × t i + 1 − t i
where: yi is an assessment of white root rot disease aerial plant symptoms at the corresponding ith evaluation day, ti is day in its corresponding ith evaluation, and n is the number of assessment days.
S A U D P C = A U D P C ∑ t
where: ∑ t is the total number of evaluation days.

2.5. Leaf Chlorophyll Content Assessment

The measurement of chlorophyll content was performed in all replicates from all R. necatrix effects and rootstocks by selecting three leaves (sub-samples) per plant. This evaluation process was carried out with an MC-100 chlorophyll meter (µmol of chlorophyll per m2 of leaf; Apogee Instruments Inc., North Logan, UT, USA) once per week (every Wednesday), starting from Rn452 inoculation until all inoculated plants from one rootstock died (269 days in total). Thus, the standardized area under the chlorophyll progress curve (SAUCPC) was calculated from all these values and adapted according to [73,74]:
A U C P C = ∑ i − 1 n − 1 y i + y i + 1 2 × t i + 1 − t i
where: yi is an assessment of chlorophyll content at the corresponding ith evaluation day, ti is the day at the corresponding ith evaluation day, and n is the total number of assessment days.
S A U C P C = A U D P C ∑ t
where: ∑ t is the total number of assessment days.

2.6. Biomass of Fresh Weight

Nine replicates per R. necatrix effect and rootstock were chosen for harvesting in three pieces (roots, stems and leaves) when the experiment finished. For each plant, stem and leaf sections were hand collected and immediately weighted with a CB-3000C digital scale (g; COBOs precision, L’Hospitalet de Llobregat, Barcelona, Spain). Each root was extracted from the pot, washed with water for removing the substrate, dried over filter paper and weighted in the digital scale. After recording the weight, all stems and roots were removed, and the leaves from each plant were kept in a paper envelope. Finally, percentage of biomass reduction (%; PBR) was calculated with the weight data from each above-ground (stems + leaves) and root section in each plant, using Vincent’s equation [75]:
P B R % = C W − T W C W × 100
where: CW is weight (g) of control plants (non-inoculated) averaged across nine replicates from fresh weight per plant section; TW is weight (g) of inoculated plants from fresh weight per plant section.

2.7. Evaluation of Leaf Area

When the experiment finished, each collected leaf sample in the paper envelope was used for measuring the leaf area using an LI-3100C area meter (cm2; LI-COR Biosciences, Lincoln, NE, USA). After this process, all leaves were removed.

2.8. Statistical Analysis

One-way analysis of variance (ANOVA) was performed for SAUDPC and PBR from both groups of plant sections (above ground (leaves + stems) and root sections). Two-way ANOVA was executed for SAUCPC and the leaf area parameters. In both cases, the free software R (version 4.1.2) was utilized [76], and the LSD-Fisher test (p < 0.05) [77] was used for separation of means with the “agricolae” package [78]. Figure 2 was plotted with the “ggplot2” [79] package by the same free software version.

3. Results

3.1. Plant Symptom Response

Results from SAUDPC showed significant differences among the assessed rootstocks (F10; 87 = 7.41 and p < 0.001). Any disease symptom was recorded in plants that were not inoculated with R. necatrix. In the case of plants inoculated with R. necatrix, the highest symptom rate (SAUDPC) was found with AMB+CZO (3.30), followed by A+VOLK × Orange 19-11-8 (3.21), UFR-4 (3.18), 2247 × 2075-01-2 (3.12), N40R1T18 (3.08), WGFT+50-7 (2.93) and N40R2T19 (2.83) without statistical differences among them. In contrast, AMB-CZO showed significant differences compared with the remaining citrus rootstocks, as did B11R3T24 (2.75), Carrizo citrange (2.67), N40R3T25 (2.05) and B11R5T25 (1.68). These last two candidates were significantly lower than the other tested rootstocks (Figure 2).

3.2. Chlorophyll Content in the Different Citrus Rootstocks

Statistical differences were detected on plant chlorophyll content under SAUCPC between the effect of R. necatrix inoculation among the citrus rootstocks and in the combination of both (effect of R. necatrix inoculation: F1; 566 = 346.92, and p < 0.001; citrus rootstock: F10; 566 = 68.67, and p < 0.001; effect of R. necatrix inoculation × citrus rootstock: F10; 566 = 6.75, p < 0.001). Additionally, the results of SAUCPC were significantly lower in inoculated plants than control plants for each rootstock, except for N40R3T25. The lowest chlorophyll rate was found in inoculated plants of A+VOLK × Orange 19-11-8 with statistical differences among the citrus rootstocks, except N40R1T18 and UFR-4. On the contrary, B11R5T25 displayed the highest significant SAUCPC among the rootstocks and inoculated plants. The remaining citrus rootstocks showed intermediate response of SAUCPC with different grades of significance among them, and between both R. necatrix effects (Table 2).

3.3. Effect of R. necatrix on the Reduction of Biomass Fresh Weight

Significant differences were obtained in the PBR results for the fresh weight of above-ground sections among the citrus rootstocks evaluated (F10; 87 = 4.86, and p < 0.001). In this sense, the highest PBR was accomplished by AMB+CZO, followed by WGFT+50-7, UFR-4 and A+VOLK × Orange 19-11-8 without statistical differences. Conversely, N40R3T25, followed by B11R5T25 and N49R2T19, displayed the lowest significant reduction of biomass compared with AMB+CZO. In addition, an intermediate PBR response was found for Carrizo citrange, N40R1T18, 2247 × 2075-01-2 and B11R3T24, with statistical differences respecting AMB+CZO and N40R3T25 (Table 3).
Regarding PBR for the fresh weight of root sections, statistical differences were detected among the rootstocks (F10; 87 = 3.68, and p < 0.001). AMB+CZO and A+VOLK × Orange 19-11-8 displayed the highest PBR, followed by WGFT+50-7, UFR-4 and Carrizo citrange without significant differences. On the contrary, the lowest PBR was achieved by N40R2T19 and B11R5T25, followed by N40R3T25, 2247 × 2075-01-2, B11R3T24 and N40R1T18 without significant differences, but were statistically different with the highest response (Table 3).

3.4. Response of Leaf Area in Different Citrus Rootstocks

In the case of leaf area response, statistical differences between the effect of R. necatrix inoculation among the citrus rootstocks and the combination of them were detected (effect of R. necatrix inoculation: F1; 168 = 80.61, and p < 0.001; citrus rootstock: F10; 168 = 17.85, and p < 0.001; effect of R. necatrix inoculation × citrus rootstock: F10; 168 = 2.12, and p = 0.025). The result of leaf area was lower in inoculated plants than control plants, which differed statistically between both effects for each citrus rootstock, except for B11R3T24, N40R1T18, N40R3T25 and 2247 × 2075-01-2. The lowest leaf area rate for inoculated and non-inoculated plants was achieved by N40R1T18, N40R3T25 and N40R2T19, followed by AMB+CZO, WGFT+50-7, B11R5T25 and B11R3T24 without statistical differences among them. On the other hand, 2247 × 2075-01-2 obtained the highest leaf area response among the rootstocks and per each effect of R. necatrix inoculation, which were statistically different compared with the lowest rate. In the control plants, this last result was followed by A+VOLK × Orange 19-11-8, B11R5T25 and Carrizo citrange without significant differences. Furthermore, an intermediate significant result of leaf area was found in A+VOLK × Orange 19-11-8, Carrizo citrange and UFR-4 for the inoculated plants, compared with the highest and lowest response (Table 4).

4. Discussion

This study has achieved the physiological response of 11 new and HLB-tolerant citrus rootstocks to WRR after artificial inoculation of R. necatrix. Proper rootstock selection is usually carried out to avoid abiotic (salinity, soil with high pH, flooding, drought and freeze) and biotic (Phytophthora, nematodes and citrus tristeza virus) diseases, as well as horticultural traits (tree size, fruit production and quality). Among these rootstocks, only AMB+CZO, UFR-4 and WGFT+50-7 have been priorly evaluated in term of fruit production and were quality grafted with ‘Hamling’ orange in two locations and during two harvest seasons (2018–19 and 2019–20) [80]. Thus, these three rootstocks displayed high ‘Hamling’ fruit production in one trial location and during both harvest seasons. In the second trial location, AMB+CZO and UFR-4 achieved high and intermediate-low fruit production during the harvested seasons of 2018–19 and 2019–20, respectively. Concerning WGFT+50-7, it showed low and intermediate-low production during 2018–19 and 2019–20, respectively. In addition, AMB+CZO, UFR-4 and WGFT+50-7 rootstocks are currently under field evaluation in two different locations of Florida by another research project [66]. All the 11 citrus rootstocks assessed in this study have been grown recently (2021) and were priorly grafted with ‘Lane Late’ cultivar in a field research plot located at “Las Torres” Center from Andalusian Institute for Agricultural and Fisheries Research and Training and Alcalá del Río municipality (37°30′52.52″ N; 55°7′59.66″ W; Seville, Spain), where agronomic traits are being evaluated, but no data have yet been recorded.
In prior research, Sztejnberg and Madar [5] demonstrated that Poncirus trifoliata displayed the highest tolerance rate under R. necatrix inoculations. In our results, the diploid rootstocks B11R5T25 and N40R3T25 achieved the lowest disease occurrence of symptoms caused by R. nectrix inoculations. Additionally, B11R5T25 showed the highest chlorophyll content in both effects of R. necatrix, and the lowest PBR response for both sections were found in N40R3T25, N40R2T19 and B11R5T25. On the contrary, these three diploid rootstocks obtained low leaf area rates. In this sense, B11R5T25 and N40R3T25 have the same direct parent, which is P. trifoliata. Similarly, a recent study carried out by this group identified two other new HLB-tolerant citrus rootstocks with the slightest incidence of WRR; in addition P. trifoliata constitutes a direct parent in the cross of those both candidates [35].
In Spain, Carrizo citrange is the most cultivated rootstock with a frequency of 61% [81], causing a low diversity rate of plant material among the citrus orchards. Therefore, we include this rootstock as the standard-comparative as it shares a common parent (P. trifoliata) with B11R5T64 and B11R5T60, but it displayed an intermediate response against WRR in this present study. Although Sztejnberg and Madar [5] did not assess Carrizo citrange, they found an intermediate R. necatrix incidence in Troyer citrange (Citrus sinensis ‘Washington’ × P. trifoliata), which is usually described as being exactly alike [64,82]. Otherwise, Carrizo citrange was reported as one of the most susceptible rootstocks to WRR after artificial inoculations were compared with other new HLB-tolerant citrus rootstocks [35]. On the other hand, AMB+CZO and A+VOLK × Orange 19-11-8 accomplished the highest disease incidence in symptoms and the second one displayed the lowest chlorophyll content under the inoculated effect of R. necatrix, and the highest PBR was found in both of these tetraploid rootstocks for root sections, where this pathogen directly infected the plant. Concerning leaf area, the highest rate was achieved by 2247 × 2075-01-2 in plants with both R. necatrix effects.
In previous work related to the susceptibility of citrus rootstocks to R. necatrix disease, Sztenjnberg and Madar [5] found one rootstock from a total of four with the highest tolerance against WRR (25%), and Arjona-López et al. [35] found two from a total of 12 (16.7%). In this current study, we also identified two rootstocks with the highest tolerance to WRR from a total of 11 tested candidates (18.2%); thus, the successes percentage is between those of both prior studies. Regarding other fruit trees, our success percentage (18.2%) is higher than in other investigations, such as apple (2.8%) [36], avocado (0.3% and 1.5%) [38,83] and persimmon rootstock “Diospyros virginiana”, but lower than the persimmon rootstock “D. kaki” [41,42].

5. Conclusions

In our findings, we characterized physiological susceptibility of several new HLB-tolerant citrus rootstocks inoculated by R. necatrix. In total, we found two interesting candidates (B11R5T25 and N40R3T25) with the highest tolerance rate to WRR. Therefore, these two rootstocks could be interesting future choices for growers with R. necatrix problems in their orchards and/or for breeding programs in the development of new technology.

Author Contributions

Conceptualization, J.M.A.-L. and F.J.A.-A.; methodology, J.M.A.-L. and F.J.A.-A.; software, J.M.A.-L., J.L.C.-S. and E.R.-R.; validation, J.M.A.-L. and F.J.A.-A.; formal analysis, J.M.A.-L.; investigation, J.M.A.-L., J.L.C.-S. and E.R.-R.; resources, F.G.G.J., J.W.G., C.J.L.-H. and F.J.A.-A.; data curation, J.M.A.-L., J.L.C.-S. and E.R.-R.; writing—original draft preparation, J.M.A.-L.; writing—review and editing, F.G.G.J., J.W.G., C.J.L.-H. and F.J.A.-A.; visualization, J.M.A.-L. and F.J.A.-A.; supervision, J.M.A.-L. and F.J.A.-A.; project administration, J.M.A.-L. and F.J.A.-A.; funding acquisition, F.J.A.-A. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors are highly thankful to Agromillora Group for providing the plant material, including Mariàngela Mestre and Joan Torrent, and to the “Juan de la Cierva-training” postdoctoral grant 2021 (FJC2021-047313-I) from Spanish Ministry of Science and Innovation (Ministerio de Ciencia e Innovación). We are also grateful for the technical assistance of Carlos Casanova (Institute for Sustainable Agriculture, Spanish Research Council), Oliva Inmaculada López Castrillón and José Antonio Monferrer Salinas.

Conflicts of Interest

The authors declare no conflict of interest.

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Horticulturae 09 00744 g001 550
Figure 1. Disease symptom scale of 1–5: 1, healthy plant; 2, first signs of leaf decline and chlorosis on plant; 3, plant with chlorotic and curly leaves; 4, wilted plant with first symptoms of leaf desiccation; and 5, dead plant.
Figure 1. Disease symptom scale of 1–5: 1, healthy plant; 2, first signs of leaf decline and chlorosis on plant; 3, plant with chlorotic and curly leaves; 4, wilted plant with first symptoms of leaf desiccation; and 5, dead plant.
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Horticulturae 09 00744 g002 550
Figure 2. Mean standardized area under the disease progress curve (SAUDPC) ± standard error (SE) in inoculated plants from 11 citrus rootstocks (Carrizo citrange, B11R3T24, B11R5T25, N40R1T18, N40R2T19, N40R3T25, A+VOLK × Orange 19-11-8, AMB+CZO, UFR-4, WGFT+50-7 and 2247 × 2075-01-2). Values in columns with different letters denote statistical differences among citrus rootstocks assayed by LSD-Fisher’s test (p < 0.05).
Figure 2. Mean standardized area under the disease progress curve (SAUDPC) ± standard error (SE) in inoculated plants from 11 citrus rootstocks (Carrizo citrange, B11R3T24, B11R5T25, N40R1T18, N40R2T19, N40R3T25, A+VOLK × Orange 19-11-8, AMB+CZO, UFR-4, WGFT+50-7 and 2247 × 2075-01-2). Values in columns with different letters denote statistical differences among citrus rootstocks assayed by LSD-Fisher’s test (p < 0.05).
Horticulturae 09 00744 g002
Table
Table 1. HLB-tolerant citrus rootstocks assayed against R. necatrix infection in this study.
Table 1. HLB-tolerant citrus rootstocks assayed against R. necatrix infection in this study.
RootstockParentageBreederReferences
Diploids
Carrizo citrangeCitrus sinensis ‘Washington’ × Poncirus trifoliataUSDA[64]
B11R3T24P. trifoliata × C. paradisi ‘Duncan’CREC[65]
B11R5T25P. trifoliata × C. paradisi ‘Duncan’CREC[65]
N40R1T18P. trifoliata ‘Flying Dragon’ × (C. clementina × C. paradisi ‘Duncan’)CREC[66]
N40R2T19P. trifoliata ‘Flying Dragon’ × (C. clementina × C. paradisi ‘Duncan’)CREC[66]
N40R3T25P. trifoliata ‘Flying Dragon’ × (C. clementina × C. paradisi ‘Duncan’)CREC[65]
Tetraploids
A+Volk × Orange 19-11-8 aC. volkameriana × (C. reticulata ‘Nova’ + C. maxima ‘Hirado Buntan’ × C. reticulata ‘Cleopatra’+ P. trifoliata)CREC[67]
AMB+CZO bC. amblycarpa+Citroncirus spp. ‘Carrizo’CREC[68]
UFR-4 aC. reticulata ‘Nova’ + C. Maxima ‘Hirado Buntan’ × C. reticulata ‘Cleopatra’ + P. trifoliataCREC[69,70]
WGFT+50-7 bC. paradisi ‘White’ + P. Trifoliata ‘50-7′CREC[71]
2247 × 2075-01-2 aC. reticulata ‘Nova’ + C. Maxima ‘Hirado Buntan’ × C. reticulata ‘Cleopatra’ + Citroncirus spp. ‘Swingle’CREC[65]
a: tetrazyg; b: somatic hybrid; +: indicates somatic hybridization (allotetraploid); ×: indicates sexual hybridization (diploid or tetraploid); CREC: Citrus Research and Education Center, University of Florida (Lake Alfred, FL, USA); USDA: United States Department of Agriculture (Riverside, CA, USA).
Table
Table 2. Mean standardized area under the chlorophyll progress curve (SAUCPC) ± standard error (SE) due to the effect of R. necatrix infection (inoculated and control (non-inoculated)) on leaf chlorophyll content in plants from 11 citrus rootstocks (Carrizo citrange, B11R3T24, B11R5T25, N40R1T18, N40R2T19, N40R3T25, A+VOLK × Orange 19-11-8, AMB+CZO, UFR-4, WGFT+50-7 and 2247 × 2075-01-2).
Table 2. Mean standardized area under the chlorophyll progress curve (SAUCPC) ± standard error (SE) due to the effect of R. necatrix infection (inoculated and control (non-inoculated)) on leaf chlorophyll content in plants from 11 citrus rootstocks (Carrizo citrange, B11R3T24, B11R5T25, N40R1T18, N40R2T19, N40R3T25, A+VOLK × Orange 19-11-8, AMB+CZO, UFR-4, WGFT+50-7 and 2247 × 2075-01-2).
RootstockEffect of R. necatrix Inoculation
InoculatedControl (Non-Inoculated)
Carrizo citrange506.87 ± 30.56 d695.34 ± 15.66 bc
B11R3T24453.02 ± 27.64 de630.90 ± 30.81 c
B11R5T25628.72 ± 34.27 c773.97 ± 18.92 a
N40R1T18256.96 ± 14.24 ij328.68 ± 6.61 gh
N40R2T19285.84 ± 13.25 hi416.25 ± 15.02 ef
N40R3T25334.26 ± 18.25 gh381.12 ± 16.52 fg
A+VOLK × Orange 19-11-8212.23 ± 26.22 j404.08 ± 10.89 ef
AMB+CZO370.47 ± 35.48 fg715.05 ± 18.13 ab
UFR-4261.74 ± 30.57 ij495.88 ± 17.29 d
WGFT+50-7449.41 ± 31.30 de716.48 ± 19.72 ab
2247 × 2075-01-2405.34 ± 35.36 ef655.88 ± 18.80 bc
Values with different letters denote statistical differences among citrus rootstocks and between the effects of R. necatrix inoculation assessed by LSD-Fisher’s test (p < 0.05).
Table
Table 3. Mean percentage of biomass reduction (%) ± standard error (SE) in inoculated plants as fresh weight above ground (leaves + stems) and root sections in plants from 11 citrus rootstocks (Carrizo citrange, B11R3T24, B11R5T25, N40R1T18, N40R2T19, N40R3T25, A+VOLK × Orange 19-11-8, AMB+CZO, UFR-4, WGFT+50-7 and 2247 × 2075-01-2).
Table 3. Mean percentage of biomass reduction (%) ± standard error (SE) in inoculated plants as fresh weight above ground (leaves + stems) and root sections in plants from 11 citrus rootstocks (Carrizo citrange, B11R3T24, B11R5T25, N40R1T18, N40R2T19, N40R3T25, A+VOLK × Orange 19-11-8, AMB+CZO, UFR-4, WGFT+50-7 and 2247 × 2075-01-2).
RootstockPlant Section
Above GroundRoots
Carrizo citrange24.11 ± 4.58 bcde52.78 ± 6.13 abcd
B11R3T2416.94 ± 6.03 de34.99 ± 6.07 cde
B11R5T2510.61 ± 5.96 ef28.94 ± 9.58 e
N40R1T1821.26 ± 4.10 cde38.28 ± 8.05 bcde
N40R2T1910.72 ± 7.07 ef27.17 ± 7.29 e
N40R3T250.00 ± 0.00 f33.76 ± 6.02 de
A+VOLK × Orange 19-11-833.11 ± 8.70 abcd59.63 ± 6.08 a
AMB+CZO44.70 ± 8.62 a69.10 ± 5.41 a
UFR-438.61 ± 8.20 abc55.08 ± 10.62 abc
WGFT+50-740.45 ± 5.51 ab58.81 ± 4.92 ab
2247 × 2075-01-218.63 ± 6.82 de34.29 ± 10.53 cde
Values with different letters denote statistical differences among the citrus rootstocks assessed for each plant section by LSD-Fisher’s test (p < 0.05).
Table
Table 4. Mean leaf area response (cm2) ± standard error (SE) due to the effect of R. necatrix infection (inoculated and control (non-inoculated)) in plant leaves from 10 citrus rootstocks (Carrizo citrange, B11R3T24, B11R5T25, N40R1T18, N40R2T19, N40R3T25, A+VOLK × Orange 19-11-8, AMB+CZO, UFR-4, WGFT+50-7 and 2247 × 2075-01-2).
Table 4. Mean leaf area response (cm2) ± standard error (SE) due to the effect of R. necatrix infection (inoculated and control (non-inoculated)) in plant leaves from 10 citrus rootstocks (Carrizo citrange, B11R3T24, B11R5T25, N40R1T18, N40R2T19, N40R3T25, A+VOLK × Orange 19-11-8, AMB+CZO, UFR-4, WGFT+50-7 and 2247 × 2075-01-2).
RootstockEffect of R. necatrix inoculation
InoculatedControl (Non-Inoculated)
Carrizo citrange403.23 ± 101.98 efgh993.88 ± 106.44 ab
B11R3T24281.75 ± 70.67 fghij474.21 ± 52.37 efg
B11R5T25261.60 ± 83.08 fghij1030.81 ± 105.52 ab
N40R1T180.00 ± 0.00 j64.78 ± 36.80 hij
N40R2T1931.85 ± 16.53 j526.38 ± 106.50 def
N40R3T2514.60 ± 6.25 j56.99 ± 17.41 ij
A+VOLK × Orange 19-11-8643.41 ± 219.16 cde1209.94 ± 121.05 a
AMB+CZO172.22 ± 56.43 ghij624.09 ± 69.94 cde
UFR-4360.10 ± 79.87 efghi794.91 ± 139.64 bcd
WGFT+50-7231.31 ± 78.13 fghij873.31 ± 61.34 bc
2247 × 2075-01-2952.26 ± 244.26 ab1245.27 ± 154.22 a
Values with different letters denote statistical differences among citrus rootstocks and between the effects of R. necatrix inoculation assessed by LSD-Fisher’s test (p < 0.05).
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MDPI and ACS Style

Arjona-López, J.M.; Gmitter, F.G., Jr.; Romero-Rodríguez, E.; Grosser, J.W.; Cantero-Sánchez, J.L.; López-Herrera, C.J.; Arenas-Arenas, F.J. Plant Physiological Assessments on Promising New HLB-Tolerant Citrus Rootstocks after Inoculation with the Phytopathogenic Ascomycete Rosellinia necatrix. Horticulturae 2023, 9, 744. https://doi.org/10.3390/horticulturae9070744

AMA Style

Arjona-López JM, Gmitter FG Jr., Romero-Rodríguez E, Grosser JW, Cantero-Sánchez JL, López-Herrera CJ, Arenas-Arenas FJ. Plant Physiological Assessments on Promising New HLB-Tolerant Citrus Rootstocks after Inoculation with the Phytopathogenic Ascomycete Rosellinia necatrix. Horticulturae. 2023; 9(7):744. https://doi.org/10.3390/horticulturae9070744

Chicago/Turabian Style

Arjona-López, Juan M., Frederick G. Gmitter, Jr., Estefanía Romero-Rodríguez, Jude W. Grosser, José Luís Cantero-Sánchez, Carlos J. López-Herrera, and Francisco J. Arenas-Arenas. 2023. "Plant Physiological Assessments on Promising New HLB-Tolerant Citrus Rootstocks after Inoculation with the Phytopathogenic Ascomycete Rosellinia necatrix" Horticulturae 9, no. 7: 744. https://doi.org/10.3390/horticulturae9070744

APA Style

Arjona-López, J. M., Gmitter, F. G., Jr., Romero-Rodríguez, E., Grosser, J. W., Cantero-Sánchez, J. L., López-Herrera, C. J., & Arenas-Arenas, F. J. (2023). Plant Physiological Assessments on Promising New HLB-Tolerant Citrus Rootstocks after Inoculation with the Phytopathogenic Ascomycete Rosellinia necatrix. Horticulturae, 9(7), 744. https://doi.org/10.3390/horticulturae9070744

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