Resistance in potato to two haplotypes of ‘Candidatus Liberibacter solanacearum’

  • María Guadalupe Hernández-Deheza
  • Reyna Isabel Rojas-Martínez
  • Antonio Rivera-Peña
  • Emma Zavaleta-Mejía
  • Daniel Leobardo Ochoa-Martínez
  • Alfredo Carrillo-Salazar
Original Article
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Abstract

The disease zebra chip (ZC) caused by the bacterium Candidatus Liberibacter solanacearum causes important economic losses in potato in New Zealand, the United States, Mexico and Central America; in Mexico, haplotypes LsoA and LsoB of the bacterium have been found in chili and potato. The pathogen is transmitted by the psyllid Bactericera cockerelli, and the presence of internal marking in the form of necrotic striation in the medulla of the tubers is considered a typical diagnostic symptom. The potato cultivars currently grown in Mexico are susceptible to this bacterium. The present study evaluates the responses of potato cultivars Atlantic (highly susceptible control), Milagros, one new entry, Real 14, and the experimental clones Bajio 143 and T05–20-11 to inoculation with two haplotypes of the bacterium over two production cycles. The plants inoculated with the mixture of LsoA and LsoB haplotypes, compared with inoculation with only LsoB, showed greater severity of foliar damage and area below the curve of progress of the disease, but not of necrosis in tubers (with exception of cv. Milagros). The cv. Real 14 showed a lower percentage of tuber discolouration than three other tested cultivars after inoculation with the mixture of haplotypes, and less than cvs Atlantic and Bajio 143, after inoculation with LsoB. The same cultivar expressed significantly less severe plant symptoms than cv. Atlantic. The clone T05–20-11 showed significantly less severe tuber symptoms than cv. Atlantic, after inoculation with mixed haplotypes and less severe symptoms than cvs Atlantic and Bajio 143 after, inoculation with LsoB.

Keywords

Bactericera cockerelli LsoA LsoB LsoA+LsoB Resistance Zebra chip 

Introduction

Potato (Solanum tuberosum) is grown in more than 130 countries and is the fourth most important crop cultivated in the world (FAO 2016), after wheat (Triticum aestivum), rice (Oryza sativa) and maize (Zea mays L.). In Mexico, potato occupies the fifth place in area sown (65,000 ha) with an annual average production of 1.7 million tonnes. The main production States are: Sinaloa, Sonora, Nuevo León, Chihuahua, Zacatecas, Guanajuato, Michoacán, Puebla and the State of México (SIAP 2016).

The oomycete Phytophthora infestans is the most important pathogen on this crop; however, in recent years the disease known as zebra chip, caused by the bacterium Candidatus Liberibacter solanacearum (CaLso), has caused important losses, reported in 2008 from New Zealand (Liefting et al. 2008, 2009) and subsequently in the United States, Mexico and Central America (Munyaneza et al. 2011).

In the family Solanaceae the bacterium is transmitted by the psyllid Bactericera cockerelli (Liefting et al. 2008), causing chlorosis, deformation of the stems, veins growing in a zigzag form, development of aerial tubers, darkening of the vascular system, and folding or withering of the leaves. In potato, the presence of necrotic striation in the medulla of the tubers (a change known commonly as zebra chip) is considered diagnostic for this disease (Munyaneza et al. 2007; Liefting et al. 2008, 2009). Five haplotypes of CaLso have been identified: two in Solanaceae (LsoA and LsoB), the third and fourth in carrot (Daucus carota) in Finland (LsoC) and in Spain (LsoD) respectively, and a fifth (LsoE) in celery (Apium graveolens) (Nelson et al. 2011, 2012). In Mexico, Rojas-Martínez et al. (2016) reported the presence of haplotypes LsoA and LsoB in chili in Yurecuaro (Mich.), and haplotype LsoB in potato in Toluca (State of Mexico); these occurrences were of individual haplotypes on the hosts with no occurrence of combinations of haplotypes.

All of the commercial potato cultivars grown in Mexico are susceptible to the bacterium, so the management of CaLso is based principally on the chemical control of the insect vector because the application of antibiotics does not achieve any remission of the symptoms or the death of the bacterium (Khairulmazmi et al. 2008; Munyaneza 2015). An alternative for the management of this disease is a search for potato lines resistant to the bacterium in combination with environment friendly cultural practices.

Based on the foregoing, the present investigation assessed the infection by two haplotypes of Candidatus Liberibacter solanacearum (LsoA and LsoB) of five genotypes of potato, two of which are experimental clones obtained in a program of genetic improvement of potato with both wild species and commercial cultivars as parents.

Materials and methods

Plant material

The experiment was set up in a greenhouse in Montecillo, State of Mexico (19.45° N, 98.9° W and altitude 2220 m) over two cropping cycles of summer-winter 2015 and 2016. There were 30 treatment combinations of the five potato genotypes (G) with three combinations of haplotypes of the bacterium (H) and two cropping cycles (C). The potato genotypes included two experimental clones (T05–20-11 and Bajío143), one new cultivar Real 14 and the commercial cvs Milagros and Atlantic (highly susceptible control). The plants were inoculated with haplotype LsoB or a combination of haplotypes LsoA and LsoB, and the control plants were left uninoculated.

In each cropping cycle, a single tuber was sown in each experimental unit, wich consisted of bags of 1.5 l capacity filled with a 2:1 mixture of peat moss/agrolite. Fertilization was applied with a mixture recommended for potato (170 N-210P-170 K + Ca,+ S,+ Mg + B) at a rate of 100 g/l and Captan was applied at the manufacturer’s recommended rate at planting and at 20 days after planting. The experiment was set out in a randomized block design with eight replicates, each experimental unit consisting of one plant. The plants were maintained in a cage measuring 3 × 2.5 m and 1.5 m high, covered with anti-aphid netting.

Reproduction of Bactericera cockerelli

Two colonies of insects, one infected with haplotype LsoB and the other with the combination LsoA+LsoB, were established on tomato plants (Solanum lycopersicum cv. Río Grande). The plants were maintained inside entomological cages at 25 ± 2 °C, 40% RH and a photoperiod of 18 h light.

Transmission of ‘Candidatus Liberibacter solanacearum’

At 30 days after planting, the tomato plants were covered individually with anti-aphid nets. Adults of B. cockerelli were collected with an insect aspirator from the colonies with haplotype LsoB or the combination of LsoA+LsoB. Adults from one or other of the colonies were introduced inside the nets of each experimental unit, according to the experimental design, were left in place for 48 h and then eliminated.

Variables analyzed

Severity (SV). The severity of symptoms on the foliage of the plants was evaluated weekly, from the first week after inoculation with the haplotypes until harvesting of the plants. For this evaluation, a scale of 1 to 5 proposed by Rivera-Peña (A. Rivera-Peña, personal communication) was used, with some modifications, where 1 = plant asymptomatic (0%); 2 = rolling of the leaves and yellowing of the plant (25%); 3 = stunting, rolling of leaves and yellowing of the plant (50%); 4 = aerial tubers and rolling of the whole plant, stunting, and occasional purple leaves (75%); 5 = death of the plant (100%).

Disease intensity. The number of plants with symptoms of zebra chip (ZC) were recorded weekly, and the area beneath the curve of the progress of the disease (AUDPC) was calculated using the formula proposed by Shaner and Finney (1977).

Yield and its components. All of the tubers produced by each plant were weighed to determine the yield of each plant (YP) and the number of tubers per plant was counted (NTP); the equatorial diameter of each tuber was measured and the tubers were classified into five categories (classification of tubers, CLT): large (>56 mm), first class (45 to 55 mm), second (35 to 44 mm), third (28 to 34 mm) and fourth or waste (<28 mm).

Tuber discolouration (TD). Five tubers were taken from each plant, each one was cut in half and from each half two slices of approximately two mm thickness were taken. The slices were fried in sunflower oil for five min at 180 °C in an electric fryer (Frinox the Turmix model FP-8). Photographs were then taken with a 13 megapixel camera under constant white light and saved in jpeg format for analysis based on a diagrammatic scale of an artificial neuronal network (methodology in the process of publication).

Statistical analysis

Data for the variables SV, AUDPC, YP, NTP and CLT were submitted to analysis of variance (ANOVA) and means were separated by Tukey’s test (P ≤ 0.05) using the SAS statistical program. Analysis of the variable TD was done by t test for pairs with the correction of Bonferroni (Holm 1979).

Results

Significant (P ≤ 0.05) differences were found between cropping cycles for the variables AUDPC, CLT and TD; between genotypes for SV, NTP and TD; between haplotype treatments for SV, AUDPC and TD; and for the interactions CxG, GxH and CxGxH in the variable TD but in CxH only for the AUDPC (Table 1).
Table 1

Squared means from the analysis of variance performed on five genotypes of potato inoculated with two haplotypes of Candidatus Liberibacter solanacearum (CaLso) in two cropping cycles

FV

DF

SV

AUDPC

YP

NTP

CLT

DF¥

TD

C

1

0.1

16.5*

0.3

0.0

18.4*

1

137.5*

G

4

8.3*

1.2

0.4

9.7*

5.2

4

70.1*

H

2

27.1*

34.3*

0.9

0.1

0.5

2

151.7*

CxG

4

7.3

3.9

0.5

0.2

0.8

4

13.2*

CxH

2

5.8

12.3*

2.0

0.2

0.0

2

8.9

GxH

8

0.7

1.5

1.1

1.2

1.2

8

21.3*

CxGxH

6

1.5

0.7

0.3

0.6

0.5

4

20.8*

CV (%)

 

32

35

46

48

22

 

31

FV factor of variation, DF degrees of freedom, SV severity of symptoms, AUDPC area under the disease progress curve, YP yield/plant, NTP number of tubers per plant, CLT classification of tubers, DF ¥ degrees of freedom for the variable TD (tuber discolouration), C cropping cycle, G genotype of potato, H haplotype of CaLso, CV coefficient of variation (* = P ≤ 0.05)

In the cycle of 2015 (C1) the values of the variables AUDPC, TD and CLT were lower than those observed in 2016 (C2). In the case of variables SV, YP and NTP there was no significant difference (P ≤ 0.05) (Table 2). The temperature and relative humidity were recorded during the two cropping cycles (Table 3). At first sight no large differences between cycles were evident but analysis of the standard deviation (SD) showed that conditions in C1 were relatively stable whilst C2 showed a greater variability, principally in Tmax (SD 2.46) and RH (SD 6.11). In the case of AT, the SD value between cycles for C1 was 0.04 whilst in C2 it was 0.83; for Tmax in C1 it was 1.2 and in 2.46 in C2, i.e. double than the value in C1; for Tmin the values were close, 1.73 and 1.39, but for RH there was a large difference between cycles, 1.73 and 6.11, respectively.
Table 2

Responses of five genotypes of potato inoculated with two haplotypes of Candidatus Liberibacter solanacearum in each cropping cycle

Cycle

SV

AUDPC

YP

NTP

CLT

TD

C1

30.9a

468b

99a

10a

3b

26b

C2

26.8a

826a

89a

10a

4a

34a

Each value represents the mean of the values for the two cropping cycles. Means with the same letters are not statistically different (Tukey, 0.05)

FV factor of variation, DF degrees of freedom, SV severity of foliar symptoms (%), AUDPC area under the disease progress curve, YP yield/plant (g), NTP number of tubers per plant, CLT classification of tubers, TD tuber discolouration (%)

Table 3

Temperatures during two cropping cycles of potato (Solanum tuberosum) in Montecillo, Texcoco

 

C1 (2015)

C2 (2016)

Month

AT

Tmax

Tmin

RH

AT

Tmax

Tmin

RH

May

14.0

28.2

7.8

85.9

15.3

31.4

7.4

75.2

June

14.1

25.3

5.4

86.6

14.7

25.9

5.4

83.0

July

14.1

27.1

7.2

86.6

15.0

27.2

8.4

83.4

August

14.1

27.1

9.6

86.6

13.4

26.7

8.3

90.2

SD

0.04

1.20

1.73

0.38

0.83

2.46

1.39

6.11

C cycle, AT average temperature (°C), Tmax maximum temperature in the month (°C), Tmin minimum temperature in the month (°C), RH relative humidity, SD standard deviation

Amongst genotypes, cv. Atlantic showed the highest severity of foliage symptoms (52%), AUDPC (1247) and TD (54%). The rest of the genotypes behaved in a statistically similar manner for the variables YP and CLT (Table 4). However, clone T05–20-11 had the lowest values for severity and AUDPC (24 and 506) (Table 4). The clones T05–20-11 and Real 14 had the greatest NTP (14 tubers per plant) and cv. Atlantic had the fewest tubers (7). For TD, cvs Atlantic and Bajio 143 had the greatest percentages of tuber discolouration (54% and 46%, respectively), whilst cv. Real 14 had the lowest (7%).
Table 4

Responses of five genotypes of potato inoculated with two haplotypes of ‘Candidatus Liberibacter solanacearum’

Genotypes

SV

AUDCP

YP

NTP

CLT

TD

Real 14

34b

902

91

14a

4

7d

Milagros

28b

631

89

8b

3

36b

Atlántic

52a

1247

91

7b

3

54a

Bajío 143

25b

514

85

10ab

3

46a

T05–20-11

24b

506

111

14a

4

16c

  

ns

ns

 

ns

 

Each value represents the mean of the value for the two cropping cycles. Means with the same letters are not statistically different (Tukey, 0.05)

Susceptible cultivar; SV severity of foliar symptoms (%), AUDPC area under the disease progress curve, YP yield/plant (g), NTP number of tubers per plant, CLT classification of tubers, TD tuber discolouration (%)

The combined inoculation of LsoA+LsoB caused greater SV (46%), AUDPC (1276) and TD (43%) than the individual inoculation of haplotype LsoB (Table 5). In this investigation, the means for haplotype LsoB and the control were statistically similar for SV and AUDPC, whilst in TD there were significant differences between them (32% and 4%, respectively). Table 5 shows that there are no significant differences between the haplotypes and the control treatment since it is not related to the perfomance parameters (YP, NTP and CLT), however the leaf symptoms are related in the severity variables (SV, AUDCP and TD).
Table 5

Responses of five genotypes of potato inoculated with two haplotypes of ‘Candidatus Liberibacter solanacearum’

Haplotypes

SV

AUDCP

YP

NTP

CLT

TD

LsoB

22b

436b

78a

10a

3a

32b

LsoB+LsoA

46a

1276a

97a

10a

3a

43a

Control

21b

211b

106a

11a

3a

4c

Each value represents the mean of the values for the two cropping cycles. Means with the same letters are not statistically different (Tukey, 0.05)

SV severity of foliar symptoms (%), AUDPC area under the disease progress curve, YP yield/plant (g), NTP number of tubers per plant, CLT classification of tubers, TD tuber discolouration (%)

In the variable TD there were significant differences in the two- and three-way interactions between the factors of variation, with the exception of the interaction CxH (Table 1). The genotype Real 14 inoculated with LsoB and LsoA+LsoB had the lowest percentage of tuber discolouration compared with the rest of the genotypes evaluated. In contrast, cvs Atlantic infected with LsoA+B, Bajio 143 infected with LsoB, Milagros infected with LsoA+B and Atlantic with LsoB had the greatest percentages of TD (Table 6).
Table 6

Tuber discolouration in five genotypes of potato inoculated with two haplotypes of ‘Candidatus Liberibacter solanacearum’

Genotypes

Haplotypes (TD %)

Control (TD %)

LsoA and LsoB

LsoB

Atlantic

68.1 a

56.2 abcd

4.4 g

Milagros

63.5 abc

18.5 efg

2.9 g

Bajio 143

47.4 abcde

65.4 ab

2.1 g

T05–20-11

25.2 cdef

16.6 efg

0.4 g

Real 14

8.7 fg

6.6 fg

5.9 fg

Each value represents the mean of the values for the two cropping cycles. Means with the same letters are not statistically different (Tukey, 0.05)

TD tuber discolouration, C control (uninoculated)

Discussion

During the cycle C2 we recorded greater values of SV, AUDPC and TD compared with cycle C1 although sowing was at the same time of the year for both cycles. Differences in environmental conditions, principally the greater variability during C2, could have influenced the results. Temperature is an important element in the development of the bacterium, for temperatures below 17 °C and above 32 °C inhibit its development, so that differences in temperature affect both the incidence and severity of the disease (Munyaneza et al. 2012). Also, although the same number of individuals of B. cockerelli were added to each experimental unit, the quantity of bacteria carried and inoculated by each insect could have been different between cycles owing to the variations of temperature and RH encountered. Development of B. cockerelli is optimum at 27 °C but stops at 32 °C, and these same temperatures are favorable for the development of CaLso and for the development of disease symptoms. For this reason it is believed that there was a co-evolution of the bacterium and its insect vector with regard to temperature and relative humidity during development (Munyaneza et al. 2012), which could explain in part the differences found in the variables AUDPC and TD. In this respect, it is known that the number of insects affects the time for symptom expression which could vary depending on the initial load of bacterial inoculum that each psyllid carries (Rashed et al. 2012). However, Rashed et al. (2014) say that the disease incidence is related to the movement of the insect vector on the plant and that the severity of symptoms is independent of the bacterial load; these same investigators also indicate that there is no evidence that the potato may be more susceptible to the bacterium in a particular physiological stage, but such factors could explain the differences that are found in the variable TD.

Atlantic showed the highest disease severity, AUDPC and TD, whilst cv. Real 14 had the lowest of these. Frías et al. (2001) mention that cv. Atlantic is highly susceptible to late blight in Coahuila and Nuevo León, with a crop loss of 100%. Real 14, obtained after hybridization, clonal selection and open pollination, has shown resistance to tuber discolouration, and yields similar to commercial cultivars such as Alpha in the tests made in the valley of Toluca (Campo experimental Metepec. Instituto Nacional de Investigaciones Forestales y Agrícolas y Pecuarias. Rancho San Lorenzo Metepec SN, San Lorenzo Coacalco Metepec, 52,140 Metepec, México) (A. Rivera-Peña, personal communication) in the program of genetic improvement of potato. Mendoza-Navarrete (2010) evaluated diverse genotypes of potato and found genetic resistance to ZC in clone T05–20-11 while observing a light discolouration in the tubers (unpublished data). In the present investigation this same clone showed a low level of tuber discolouration.

The combination of haplotypes LsoA+LsoB caused greater SV and AUDPC than when haplotype LsoB was inoculated individually. This result suggests a certain degree of synergy worth further investigations. Interactions between certain pathogens in certain situations results in more severe damage than that caused by single infections, and is known as synergy (Begon et al. 2006).

Both haplotypes are found in Mexico, but not infecting the same plant species (Rojas-Martínez et al. 2016). On the other hand, Wen et al. (2013) occasionally detected both haplotypes in a single plant and in a single psyllid in Texas (USA). Diagnosis and control become more complicated when more than one haplotype is involved in disease induction.

An example of bacterial synergy is the disease known as necrosis of the medulla of tomato caused by Pseudomonas cichorii, P. corrugata, P. viridiflava, P. mediterranea, P. fluorescens, Pectobacterium atrosepticum, Pectobacterium carotovorum and Dickeya chrysanthemi. The severity of this disease increases when co-infection occurs with more than one of these bacterial species (Saygili et al. 2008). Rotting of the head of broccoli is another disease complex caused by Pectobacterium carotovorum, P. marginalis, P. fluorescens and P. viriflava, whose severity increases when co-infection occurs, although the mechanism of the increase is unknown (Canaday et al. 1991).

In this investigation we found that the LsoB haplotype was not statistically different from the control treatment in the SV, AUDCP, YP, NTP and CLT variables, suggesting that haplotype LsoB was the less severe than the mixture of the haplotype A and B (Table 5), a result that differs from those reported by Wen et al. (2013) who stated that in the USA, although no definitive phenotypical differences could be assigned to haplotypes, field observations suggest that haplotype LsoB produces a more severe and destructive disease than LsoA. Differences of temperature between the two sites, the host plant and variability between bacterial haplotypes could explain the differences from our results. In this study, we did not obtain the individual LsoA haplotype, so the evaluation of the severity of the individual haplotypes would be desirable in future studies to confirm the results of Wen et al. (2013). This may answer the question whether the high pathogenicity of the combined haplotypes LsoA and LsoB is the result of a greater severity produced solely by the LsoA, because only the haplotype LsoB did not produce severity in relation to the control treatment, or because due to synergistic effect of two mixed haplotypes.

Plants have defense mechanisms whose aim is to lessen, halt or counteract an infection. Van der Plank (1984) introduced the terms “vertical resistance” and “horizontal resistance”, the latter determined by genes of continuous variation and quantitative inheritance. Horizontal resistance does not prevent the infection of plants but it diminishes the development of infection sites in plants and delays the development of infection (Agrios 2005). The cv. Real 14 and the clone T05–20-11 showed less severe symptoms, a smaller area beneath the curve of progress of the disease, less discolouration of the tubers and a yield higher than or at least equal to that of the susceptible cultivar, which suggests that these accessions possess a certain degree of resistance, whose mechanism, however, is unknown. Defense mechanisms to infection by CaLso have not been thoroughly studied. However Rashed et al. (2013) found that whitin a week of inoculation of potato plants with CaLso, there was an accumulation of phenolic compounds, peroxidases, polyphenols, chitinases, amino acids and free sugars (sucrose, glucose and fructose). This research thus suggests, that the type of plant defense towards CaLso attack is of a non-preformed (induced) biochemical type, as it is known that some of the phenols related to disease resistance (phytoalexins) are found in plants regardless of whether they are healthy or diseased, but that their synthesis or accumulation increases after infection (Agrios 2005). Phytoalexins are produced by healthy cells adjacent to necrotic and damaged cells, in response to substances that diffuse from damaged cells. Resistance occurs when one or more phytoalexins reach a concentration sufficient to inhibit the development of the pathogen. Most phytoalexins are toxic to fungi, bacteria, nematodes and other pathogenic microorganisms and play an important and active role in the resistance of plants to pathogens (Woodward and Pegg 1986). The family Solanaceae historically occupies an important place in the research related to phytoalexins considering that the first report of the presence of these compounds was made in potato (Poiatti et al. 2009).

As a conclusive remark it can be stated that since the new cv. Real 14 shows a certain degree of resistance to CaLso, its use in breeding programs can be recommended.

Notes

Acknowledgements

We appreciate the help of Dr. Ken Evans, Rothamsted Experimental Station, Harpenden, UK, for reviewing the English.

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Copyright information

© Società Italiana di Patologia Vegetale (S.I.Pa.V.) 2018

Authors and Affiliations

  • María Guadalupe Hernández-Deheza
    • 1
  • Reyna Isabel Rojas-Martínez
    • 1
  • Antonio Rivera-Peña
    • 2
  • Emma Zavaleta-Mejía
    • 1
  • Daniel Leobardo Ochoa-Martínez
    • 1
  • Alfredo Carrillo-Salazar
    • 3
  1. 1.Postgrado en Fitosanidad-Fitopatología, Colegio de PostgraduadosTexcocoMexico
  2. 2.Campo experimental MetepecInstituto Nacional de Investigaciones Forestales y Agrícolas y PecuariasMetepecMexico
  3. 3.Postgrado en Recursos Genéticos, Colegio de PostgraduadosTexcocoMéxico

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