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CROP PHYSIOLOGY & METABOLISM

Limitation to Photosynthesis in Pratylenchus penetrans- and Verticillium dahliae-Infected Potato

^a Department of Plant Pathology, 1630 Linden Dr., University of Wisconsin, Madison, WI 53706 USA
^b Dep. of Botany, University of Wisconsin, Madison, WI 53706 USA

macguid{at}macc.wisc.edu

	ABSTRACT

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Mechanism(s) responsible for decrease in photosynthetic rates of potato (Solanum tuberosum L.) leaves infected by the fungus Verticillium dahliae (Kleb) and the nematode Pratylenchus penetrans (Cobb, Sher, Allen) have not been fully researched. Two growth chamber experiments were undertaken to determine the factors contributing to the decrease in CO₂ exchange rates of young, fully expanded leaflets of potato (cv. Russet Burbank) plants grown in pots infested with P. penetrans and/or V. dahliae. Treatments were P. penetrans-infested soil, V. dahliae-infested soil, soil infested with both the nematode and the fungus, and a noninfested control. Leaf CO₂ response curves were measured at early (16 d after inoculation [DAI]) and late (42 DAI) stages of infection for all treatments at saturating light (1500 µmol m^-2 s^-1 of photosynthetically active radiation [PAR] using a portable photosynthesis system. Carbon dioxide exchange rates were also measured at 1000, 400, and 200 µmol m^-2 s^-1 PAR to determine leaf light response. At ambient CO₂ concentration, concomitant infection by both pathogens significantly reduced C assimilation rate (A) and light use efficiency (µmoles CO₂ fixed per µmol of light used), and increased the intercellular CO₂ (C_i ) of these young leaves at 42 DAI, but not at 16 DAI. Infection by either pathogen alone had little or no effect on the leaf gas exchange parameters. Analysis of the curve relating A and C_i showed that either treatment alone did not change the initial slope of the curve at 16 DAI. A significant reduction in both the initial slope of A vs. C_i curves and A at C_i = 500 µmol mol^-1 in the jointly infected plants were noticeable at 42 DAI indicating that nonstomatal effects could explain the reduction in C assimilation rate at this late stage of disease infection. Leaf patchiness might also be a contributing factor to this phenomena in the leaves of the jointly infected plants.

Abbreviations: ATP, adenosine triphosphate • DAI, days after inoculation • PAR, photosynthetically active radiation • PED, potato early dying disease • Rubisco, carboxylase-oxygenase • RuBP, ribulose bisphosphate

	INTRODUCTION

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VERTICILLIUM DAHLIAE is a fungus that invades the xylem vessels of potato plants and causes a vascular wilt disease when soilborne inoculum exceeds a threshold level specific for a soil type and a potato cultivar. When other organisms are present, particularly the nematode Pratylenchus penetrans, the disease is manifested not only as a wilt, but as premature senescence referred to as potato early dying disease (PED) (Kotcon et al., 1985; Riedel and Rowe, 1985; Riedel et al., 1985).

Infection of plants by V. dahliae begins with the germination of the dormant propagules in the soil when stimulated by the passing root of the host plant. A growing hypha of the fungus invades the root by passing through the epidermis, cortex, and endodermis. Eventually, the fungal hyphae enter the stele and colonize the plant systemically by growing and proliferating through the xylem elements of the vascular system. Alternatively, the fungus may enter the xylem through undifferentiated tissue near the root tip. The fungus colonizes the xylem elements by means of mycelium and conidia; the latter are transported upward by the transpiration stream (Garber, 1973). Xylem colonization by the fungus increases the resistance to water flow within the plant, thus resulting in leaf water deficits that lead to reductions in leaf photosynthetic rate, leaf transpiration rate, and leaf longevity (Adams et al., 1987).

The root-lesion nematode P. penetrans commonly infects potato (Bernard and Laughlin, 1976; Brown et al., 1980; Olthof et al., 1982). It feeds on the cortical cells of roots and destroys them, creating lesions. The nematode often migrates from these damaged roots to feed on healthier tissue (Zunke, 1990). Potato growth and yield is compromised by P. penetrans as a function of nematode population density.

Synergism between V. dahliae and P. penetrans causes enhanced symptom expression when population densities of the nematode and fungus are too low to cause disease alone (Martin et al., 1982; Riedel et al., 1985; MacGuidwin and Rouse, 1990). Even before foliar symptoms are evident, concomitant infection by these two pathogens cause a synergistic reduction in leaf photosynthetic rate of Russet Burbank potato (Saeed et al., 1997a). Root injury caused by nematode feeding has been considered a likely mechanism for the synergism of V. dahliae and P. penetrans in PED. Wounded roots may either stimulate the germination of the dormant microsclerotia of the fungus by increased root exudation or facilitate access for the fungus to the vascular cylinder; these two processes also may occur together. Other theories on the synergism between the two pathogens propose that P. penetrans changes host nutrition and hormone balance (Riedel et al., 1985). It also has been suggested that the nematode supresses phytoalexins (Riedel and Rowe, 1985).

Decrease of leaf photosynthetic rate of Verticillium-infected plants has been attributed to two mechanisms. One mechanism is stomatal closure caused by disease-induced water stress (Bowden et al., 1990; Haverkort et al., 1990) that results in reduced CO₂ supply to the chloroplasts. The second mechanism is the disruption in metabolic pathways of photosynthesis, such as the reduction in the activity of ribulose bisphosphate (RuBP) carboxylase-oxygenase (Rubisco), or in the capacity to regenerate the RuBP or use adenosine triphosphate (ATP) (Farquhar and Sharkey, 1982; Pennypacker et al., 1990). Bowden et al. (1990) demonstrated reduced photosynthetic rates of potato plants infected by only V. dahliae. They concluded that the initial decrease brought about by V. dahliae was caused by stomatal closure. Haverkort et al. (1990) demonstrated that decrease in photosynthetic rates of Verticillium-infected potato plants resulted from drought stress in the leaves.

The reduction in CO₂ assimilation rate of potato brought about by coinfection with V. dahliae and P. penetrans observed in our earlier studies (Saeed et al., 1997a, 1997b) was speculated to be due at least in part to stomatal closure. The objective of this study was to investigate further the mechanism(s) contributing to the decrease in C assimilation in Russet Burbank potato infected by both P. penetrans and V. dahliae.

	Materials and methods

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Plant Culture and Growth Conditions
Two experiments were conducted in a growth chamber at the University of Wisconsin Biotron, a controlled plant growth facility. Treatments were P. penetrans (P) (four nematodes cm^-3 of soil), V. dahliae (V) (40 propagules g^-1 of soil), the combination of the nematode and the fungus (P+V), and a noninfested control (C). The experimental design was a randomized complete block with 4 replicates.

Plantlets of potato (Russet Burbank) were propagated from tissue culture to assure disease-free plants and uniformity. The cuttings were grown in test tubes for 20 d and then transferred to 10-cm clay pots packed with Jiffy mix. The plantlets were kept in a growth chamber at 24°C for hardening for 2 wk and were then transplanted into 20-L plastic pots containing 1:1 mixture of Plainfield loamy sand (mixed, mesic Typic Udipsamment) and vermiculite pasteurized at 75°C for 30 min. Each plant produced a single stem, which was staked to facilitate CO₂ exchange measurements. In all plants, axillary branches were pruned to three basal branches per main stem.

A Wisconsin isolate of V. dahliae (WI V-18), in vegetative compatibility group 4A (Joaquim and Rowe, 1991), was grown on sterile rye (Secale cereale L.) seed at 20°C for 5 wk. The rye seed culture was air dried for 2 wk at room temperature and then ground in a Wiley mill. Inoculum was applied to the soil mix and thoroughly incorporated by hand before soil was added to the pots. Pratylenchus penetrans isolated from potato in Wisconsin was reared on sweet corn (Zea mays L.) explants (cv. I. O. Chief) grown on Gamborg's B-5 medium without auxins or cytokinins. Nematodes were collected (Layne and MacGuidwin, 1994) and added to the pots by means of a 20-mL syringe at the time of transplanting. A depression approximately 20 cm deep and 10 cm wide was made with a trowel in the middle of the packed pot, and the nematodes were spread directly onto the soil in the hole. The ratio of juveniles to adults in the added inoculum was 13:7.

Light was supplied by cool white fluorescent and incandescent lamps. Incident PAR at plant height started near 300 ± 15 µmol m^-2 s^-1 and increased, due to plant growth, to 500 ± 17 µmol m^-2 s^-1 by the end of each experiment. Plants were grown under a 14-h, 25°C (±0.5) photoperiod and a 10-h, 15°C (±0.5) dark period. Relative humidity was maintained at 50 ± 5%. Plants were automatically watered to excess with 0.25 strength Hoagland's solution twice daily for the first 2 wk and then four times daily thereafter until the end of the experiment. Fresh air was continuously circulated through the growth chambers with an average ambient CO₂ level of 340 ± 5 µmol mol^-1.

Carbon Dioxide Response Curves
The terminal leaflet of young fully expanded asymptomatic leaves on the main stem were selected and tagged for the study. In each of the two experiments, light and CO₂ responses were measured twice, at 16 and 42 DAI. These two days were selected on the basis of the results of our earlier measurements (Saeed et al., 1997a, 1997b) of disease progress and leaf gas exchange throughout the growth period of potato plants infected by P. penetrans and/or V. dahliae. At 16 DAI, plants were in the latent phase of infection and exhibited no visual symptoms or reduction in gas exchange parameters in most of the leaves. At 42 DAI, disease physiological symptoms were apparent only on some of the older leaves infected by V.dahliae and in one of the control plants. Table 1 presents data from our ealier studies (Saeed et al., 1997a) showing the number of days to senescence of leaves in control plants and plants inoculated with P. penetrans and/or V. dahliae.

View this table: [in this window] [in a new window]   Table 1 Days to senescence of at least one leaf in the different leaf cohorts of potato plants.

Reconstructed Light Response Curves
Carbon dioxide response curves of leaves were measured for plants in the different treatments at light levels of 1000, 400 and 200 µmol m^-2 s^-1 PAR in a darkened room adjacent to the growth room. Light response curves at C_a = 300 µmol mol^-1 were reconstructed from the corresponding A vs. C_a response data.

Leaf Water Potential Measurements
In each experiment, leaf water potential measurements were performed following the CO₂ response measurements at 42 DAI using a pressure chamber (model 3005, SoilMoisture Equipment Corp., Santa Barbara, CA). To avoid moisture loss from leaves, the terminal leaflet was sealed in a plastic bag containing a damp piece of paper towel. The terminal leaflet and 1 to 3 cm of petiole were immediately excised with a razor blade. The petiole was placed through a custom-made silicon rubber seal (RTV-11, General Electric) with the hole molded in the shape of a potato petiole. Leaf water potentials were measured on the same leaves on which CO₂ response data were measured. The endpoint was reached when the first drop of water appeared on the excised end of the leaf petiole. A magnifying lens was used to aid in detecting the endpoint. Accuracy of measurement was estimated at ±0.05 MPa.

	Results

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Gas exchange parameters measured after equilibration of the LI-COR 6200 system, referred to as initial values, corresponded with a CO₂ concentration in the air of 300 µmol mol^-1. At 16 DAI, solitary or concomitant infections had no significant effect on the initial values of A, g_s, or C_i/C_a in both experiments. However, the initial value of A was significantly lowered by the combination treatment in comparison to the control in Exp. 2 (Table 2) . At 42 DAI, infection by both pathogens reduced the initial leaf assimilation rate by 48 and 59% of the control in Exp. 1 and 2, respectively; however, the reduction was significant only in Exp. 2 (Table 2). Concomitant infection also decreased initial leaf stomatal conductance in both experiments, but the effect was not significant . The C_i/C_a was significantly (P = 0.05) greater in the V and the P+V treatments in Exp. 2. No significant differences in C_i concentrations between the treatments was observed in Exp. 1.

View larger version (33K): [in this window] [in a new window]   Fig. 1 Carbon dioxide response curves (assimilation rate vs. intercellular CO2 concentrations) of young asymptomatic leaves on control plants (C), or plants inoculated with Verticillium dahliae (V), Pratylenchus penetrans (P), or with both pathogens (P+V) measured at (a, b) 16 DAI and (c, d) 42 DAI in Exp. 1 and 2. Each point is an average of four leaves (except treatment P+V in Exp. 2, where each point in part d is an average of three leaves because the fourth plant died due to infection). Bars are standard errors of means

At C_i = 500 µmol mol^-1, the response of A to C_i was unstable in all the leaves. This behavior might be caused by inhibition of starch synthesis in healthy potato leaves as explained by Sharkey and Vassey (1989). Since the above limitation occurs only at high C_i, it may not be related to the infection-induced decrease in photosynthesis.

The light response curve (at C_a = 300 µmol mol^-1) determined from the corresponding light response data at 1000, 400, and 200 µmol m^-2 s^-1 PAR for the different treatments in Exp. 2 are shown in Fig. 2 . Similar light response data were observed in Exp. 1 (data not shown). At 16 DAI, no difference in leaf light use efficiency was observed between the treatments in both experiments. At 42 DAI, the leaf light response in the P treatment was similar to that of the control. Leaves on plants infected with V. dahliae alone showed a slow increase in A with the increase in light. A more drastic reduction in light use efficiency was discerned in plants where both pathogens were present.

View larger version (19K): [in this window] [in a new window]   Fig. 2 Light response curves (assimilation rate vs. photosynthetically active radiation) when of young asymptomatic leaves on control plants (C) or plants inoculated with Verticillium dahliae (V), Pratylenchus penetrans (P), or with both pathogens (P+V) in Exp. 2 at (a) 16 DAI and (b) 42 DAI. Each point is an average of four leaves (except treatment P+V in part b, where each point is an average of three leaves because the fourth plant died due to infection)

View larger version (12K): [in this window] [in a new window]   Fig. 3 Assimilation rate vs. leaf water potential at 42 DAI of young asymptomatic leaves on control plants (C) or plants inoculated with Verticillium dahliae (V), Pratylenchus penetrans (P), or with both pathogens (P+V) in (a) Exp. 1 and (b) Exp. 2. Each point is an average of four leaves (except treatment P+V in Exp. 2, where each point is an average of three leaves because the fourth plant died due to infection). Bars are standard errors of means

	Discussion

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The work by Downton et al. (1988) has shown that uneven distribution of photosynthesis across the leaf (referred to as patchiness) can cause a bias in the calculation of C_i . Such bias in C_i calculation would misleadingly indicate that nonstomatal factors were limiting photosynthesis. Using ¹⁴CO₂ autoradiographs, Bowden et al. (1990) showed limited leaf patchiness in potato plants infected by V. dahliae alone. This limited patchiness was observed only in some older leaves. In our study, we employed the same system used by Bowden et al. (1990), and all measurements were made exclusively on young leaves. The presence of the nematode and the fungus together in the system caused a fundamentally different plant response to their infection than to infection by V. dahliae alone. Unless the interaction of the nematode and the fungus caused a patchiness response not observed previously in V. dahliae-infected potato plants, the data are consistent with the conclusion of a nonstomatal limitation to photosynthesis. Even if this were the case, the combined treatments of the nematode and the fungus would be causing a physiological response fundamentally different from the stomatal effect found with V. dahliae alone.

In our study at 42 DAI, a few leaves in the V. dahliae-infected potato plants showed a slight nonstomatal limitation to CO₂ assimilation. These results are not in agreement with several previous gas exchange studies that involve infection with Verticillium spp. Bowden et al. (1990) concluded that reduced photosynthetic rates of potato plants infected with V. dahliae were consistent with a mechanism of stomatal closure. In a field study, Haverkort et al. (1990) demonstrated that decreases in photosynthesis of Verticillium-infected potato plants resulted from drought stress in the leaves. In comparison, alfalfa (Medicago sativa L.) infected by V. albo-atrum exhibited reduced RuBP carboxylase activity (Pennypacker et al., 1990). The slight nonstomatal effect exhibited by some leaves on the V. dahliae-infected plants at 42 DAI is consistent with Pennypacker et al. (1990).

Results from our study showed that plants jointly infected by P. penetrans and V. dahliae exhibited significantly lower leaf water potential than control plants or plants infected with either pathogen alone. Infection by V. dahiae alone decreased leaf water potential to a lesser extent than by joint infection. We did not have A or leaf water potential data from plants subjected to drying for comparison with data from infected plants; however, earlier work by Haverkort et al. (1990) had shown that the effects of V. dahiae on potato plants were similar to those of a mild drought stress in which stomatal closure is correlated with reduction in photosynthetic rate. The drought stress caused by V. dahiae was not sufficiently severe to allow nonstomatal limitations to photosynthesis (Schapendonk et al., 1989). Reduction in the hydraulic conductivity of the xylem of Verticillium-infected plants brought about a decrease in the leaf water potential (Bowden et al., 1990). Results from our study are consistent with the hypothesis that disease-induced water stress caused by decreased plant hydraulic conductance due to plugging of the xylem vessels by the fungus was partially responsible for the decrease in photosynthetic rate.

Earlier research indicated that infection by nematodes can, but does not always, result in stomatal closure and hence, reduced CO₂ exchange of crop plants. Kotcon and Loria (1986), using 0, 1, 500, and 15000 P. penetrans nematodes per plant, found no significant effect of P. penetrans inoculum density on potato leaf water potential or transpiration rate. Kaplan et al. (1976) reported that 2000 P. penetrans per plant had no significant effect on leaf diffusive resistance of sunflower (Helianthus annuus L.) during daylight periods. In a recent study (Saeed et al., 1998), we found that in the absence of V. dahliae, P. penetrans at 0.8 to 32 nematodes cm^-3 of soil had no significant effect on photosynthetic rate of Russet Burbank potato. Results from the present study clearly showed that the response of CO₂ exchange to nematode infection alone was small. This is consistent with earlier studies discussed above.

In summary, at early stages of infection (16 DAI) results from this study showed only little decrease in photosynthetic rates of diseased leaves, indicating no evidence of nonstomatal limitation to photosynthesis. However, at 42 DAI there was strong evidence that joint infection by both pathogens reduced the initial slopes of the C response curves in young potato leaves. The nematode P. penetrans caused no effect on C assimilation of potato leaves, while infection with V. dahliae alone resulted in a slight reduction in the process. These results are consistent with a reduction in Rubisco activity or the regeneration of RuBP in the leaves of the jointly infected plants. However, the effect of leaf patchiness in C_i calculation cannot be ruled out as a source of error in leaf CO₂ response.

	ACKNOWLEDGMENTS

 
This research was supported by USDA-ARS Competitive Grant #58-1275-1-136 and USDA-NRI Competitive Grant 92-3702-7609. We thank Dr. Murray Clayton for statistical assistance.

Received for publication October 27, 1998.

	REFERENCES

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• Adams S.S., Rouse D.I., Bowden R.L. Performance of alternative versions of POTWIL: A computer model that simiulates the seasonal growth of Verticillium-infected potato (abstr.) Am. Pot. J. 1987;64:429.
• Bernard E.C., Laughlin C.W. Relative susceptibility of selected cultivars of potato to Pratylenchus penetrans. J. Nematol. 1976;8:239-242.
• Bowden R.L., Rouse D.I., Sharkey T.D. Mechanism of photosynthesis decrease by Verticillium dahliae in potato. Plant Physiol. 1990;94:1048-1055.[Abstract/Free Full Text]
• Brown M.J., Riedel R.M., Rowe R.C. Species of Pratylenchus associated with Solanum tuberosum cv Superior in Ohio. J. Nematol. 1980;12:189-192.
• Downton W.J.S., Loveys B.R., Grant W.J.R. Stomatal closure fully accounts for the inhibition of photosynthesis by abscisic acid. New Phytol. 1988;108:236-266.
• Farquhar G.D., Sharkey T.D. Stomatal conductance and photosynthesis. Annu. Rev. Plant Physiol. 1982;33:317-345.
• Garber R.H. Fungus penetration and development. In: Ranney C.D., ed. Verticillium wilt of cotton. College Station, TX: USDA-ARS-519. National Cotton Pathology Research Laboratory, 1973:69-77.
• Haverkort A.J., Rouse D.I., Turkensteen L.J. The influence of Verticillium dahliae and drought on potato crop growth 1. Effects on gas exchange and stomatal behavior of individual leaves and crop canopies. Neth. J. Plant Pathol. 1990;96:273-289.
• Joaquim T.R., Rowe R.C. Vegetative compatibility and virulence of strains of Verticillium dahliae from soil and potato plants. Phytopathology 1991;81:552-558.
• Kaplan D.T., Tatter T.A., Rhode R.A. Reduction of electrical resistance in sunflower roots infected with lesion nematodes. Physiopathology 1976;66:1262-1264.
• Kotcon J.B., Loria R. Influence of Pratylenchus penetrans on plant growth and water relations in potato. J. Nematol. 1986;18:385-392.
• Kotcon J.B., Rouse D.I., Mitchell J.E. Interactions of Verticillium dahliae, Colletotrichum coccodes, Rhizoctonia solani, and Pratylenchus penetrans in the early dying syndrome of Russet Burbank potatoes. Phytopathology 1985;75:68-74.
• Layne T.L., MacGuidwin A.E. Recovery of Pratylenchus penetrans from plant tissue cultures. (Abstr.) J. Nematol. 1994;26:557.
• MacGuidwin A.E., Rouse D.I. Role of Pratylenchus penetrans in the potato early dying disease of Russet Burbank potato. Phytopathology 1990;80:1077-1082.
• Martin M.J., Riedel R.M., Rowe R.C. Verticillium dahliae and Pratylenchus penetrans: Interactions in early dying complex of potato in Ohio. Phytopathology 1982;72:640-644.
• Olthof Th.H.A., Anderson R.V., Squire S. Plant-parasitic nematodes associated with potatoes (Solanum tuberosum L.) in Simcoe County, Ontario. Can. J. Plant Pathol. 1982;4:389-391.
• Pennypacker B.W., Knievel D.P., Leath K.T., Pell E.J., Hill R.R., Jr. Analysis of photosynthesis in resistant and susceptible alfalfa clones infected with Verticillium albo-atrum. Phytopathol. 1990;80:1300-1306.
• Riedel R.M., Rowe R.C. Lesion nematode involvement in potato early dying disease. Am. Potato J. 1985;62:163-171.
• Riedel R.M., Rowe R.C., Martin M.J. Differential interactions of Pratylenchus crenatus, P. penetrans, and P. scribneri with Verticillium dahliae in potato early dying disease. Phytopathol. 1985;75:419-422.
• Saeed I.A.M., MacGuidwin A.E., Rouse D.I. Synergism of Pratylenchus penetrans and Verticillium dahliae manifested by reduced gas exchange in potato. Phytopathol. 1997;87:435-439 a.
• Saeed I.A.M., MacGuidwin A.E., Rouse D.I. Disease progress based on effects of Verticillium dahliae and Pratylenchus penetrans on gas exchange in Russet Burbank potato. Phytopathol. 1997;87:440-445 b.
• Saeed I.A.M., MacGuidwin A.E., Rouse D.I. Effect of initial nematode population density on the interaction of Pratylenchus penetrans and Verticillium dahliae on `Russet Burbank' potato. J. Nematol. 1998;30:100-107.
• SAS Institute. 1988. SAS/STAT user's guide. Release 6.03 ed.SAS Inst., Cary, NC.
• Schapendonk A.H.C.M., Spitter C.J.T., Grover P.J. Effects of water stress on photosynthesis and chlorophyll fluorescence of five potato cultivars. Potato Res. 1989;32:17-32.
• Sharkey T.D., Vassey T.L. Low oxygen inhibition of photosynthesis is caused by inhibition of starch synthesis. Plant Physiol. 1989;90:385-387.[Abstract/Free Full Text]
• Zunke U. Observations on the invasion and endoparasitic behavior of the root lesion nematode Pratylenchus penetrans. J. Nematol. 1990;22:309-320.

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