Plant Biol (Stuttg) 2000; 2(2): 161-167
DOI: 10.1055/s-2000-9461
Original Paper
Georg Thieme Verlag Stuttgart ·New York

Infection with Phloem Limited Abutilon Mosaic Virus Causes Localized Carbohydrate Accumulation in Leaves of Abutilon striatum: Relationships to Symptom Development and Effects on Chlorophyll Fluorescence Quenching During Photosynthetic Induction

G. Lohaus 1 , H. W. Heldt 1 , C. B. Osmond 2
  • 1 Biochemie der Pflanze, Albrecht-von-Haller-Institut für Pflanzenwissenschaften, Universität Göttingen, Göttingen, Germany
  • 2 Photobioenergetics Group, Research School of Biological Sciences, Institute of Advanced Studies, The Australian National University, Weston Creek, Australia
Further Information

Publication History

September 6, 1999

January 11, 2000

Publication Date:
31 December 2000 (online)

Abstract:

Infection with phloem limited Abutilon Mosaic Virus caused localized carbohydrate accumulation (high levels of starch, sucrose, and hexoses) in leaves of Abutilon striatum during early symptom development. In mature leaves with attenuated symptoms, tissues showing faint vein-clearing had markedly higher carbohydrate contents than uniformly green areas of the same leaf. A similar pattern of carbohydrate accumulation was found in pale-green mosaics in mature leaves with overt symptoms when compared to green-islands of the same leaf, but overnight carbohydrate loses were comparable to controls. Because leaves with attenuated symptoms showed no further symptom development whereas the pale-green mosaics became yellow and eventually necrotic in leaves with overt symptoms, it seems unlikely that carbohydrate accumulation following impaired translocation was responsible for symptom expression. High carbohydrate status in leaves with attenuated symptoms had little effect on nonphotochemical quenching during early stages of photosynthetic induction. In leaves with overt symptoms, areas of high carbohydrate status with pale-green mosaics showed markedly slower nonphotochemical quenching. Early symptom areas of young leaves, and advanced symptom areas of mature leaves had low starch contents but were otherwise similar to controls in carbohydrate status. Impaired nonphotochemical quenching in these tissues tended to reflect the state of symptom development, rather than carbohydrate status. Plants with overt symptoms grew about half as fast as plants with attenuated symptoms.

Abbreviations:

AbMV: Abutilon Mosaic Virus Chl: chlorophyll FM: maximum Chl fluorescence in the first saturating pulse after dark-adaptation FMŒ: maximum Chl fluorescence in subsequent saturating pulses applied during transients NPQ: nonphotochemical quenching (FM/FMŒ − 1)

References

  • 01 Balachandran,  S.,, Hurry,  V. M.,, Kelley,  S. E.,, Osmond,  C. B.,, Robinson,  S. A.,, Rohozinski,  J.,, Seaton,  G. G. R.,, and Sims,  D. A.. (1997);  Concepts of biotic stress. Some insights into the stress physiology of virus-infected plants, from the perspective of photosynthesis.  Physiol. Plant.. 100 203-213
  • 02 Balachandran,  S.,, Osmond,  C. B.,, and Daley,  P. F.. (1994);  Diagnosis of¿the earliest strain-specific interactions between tobacco mosaic¿virus and chloroplasts of tobacco leaves in vivo by means of chlorophyll fluorescence imaging.  Plant Physiol.. 104 1059-1065
  • 03 Blechschmidt-Schneider,  S.,, Ferrar,  P. J.,, and Osmond,  C. B.. (1989);  Control of photosynthesis by the carbohydrate level in source leaves of the C4 plant Amaranthus edulis. .  Planta. 177 515-525
  • 04 Bro,  E.,, Meyer,  S.,, and Genty,  B.. (1996);  Heterogeneity of leaf CO2 assimilation during photosynthetic induction.  Plant Cell Environ.. 19 1349-1358
  • 05 Daley,  P. F.. (1995);  Chlorophyll fluorescence analysis and imaging in plant stress and disease.  Canad. J. Plant Pathol.. 17 167-173
  • 06 Durnford,  D. G., and Falkowski,  P. G.. (1997);  Chloroplast redox regulation of nuclear gene transcription during photoacclimation.  Photosynth. Res.. 53 229-241
  • 07 Funayama,  S.,, Hikosaka,  K.,, and Yahara,  T.. (1997 a);  Effects of virus infection and growth irradiance on fitness components and photosynthetic properties of Eupatorium makinoi (Compositae).  Amer. J. Bot.. 84 823-829
  • 08 Funayama,  S.,, Sonoike,  K.,, and Terashima,  S.. (1997 b);  Photosynthetic properties of Eupatorium makinoi infected by a geminivirus.  Photosynth. Res.. 53 253-261
  • 09 Goldschmidt,  E. E., and Huber,  S. C.. (1992);  Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars.  Plant Physiol.. 99 1443-1448
  • 10 Heineke,  D.,, Wildenberger,  K.,, Sonnewald,  U.,, Wilmitzer,  L.,, and Heldt,  H. W.. (1994);  Accumulation of hexoses in leaf vacuoles: studies with transgenic tobacco plants expressing yeast-derived invertase in the cytosol, vacuole, or apoplasm.  Planta. 194 29-33
  • 11 Höfer,  P.,, Bedford,  I. D.,, Markham,  P. G.,, Jeske,  H.,, and Frischmuth,  T.. (1997);  Coat protein gene replacement results in white fly transmission of an insect nontransmissible geminivirus isolate.  Virology. 236 288-295
  • 12 Horns,  T., and Jeske,  H.. (1991);  Localization of Abutilon mosaic virus (AbMV) DNA within leaf tissues by in situ hybridization.  Virology. 181 580-588
  • 13 Ingham,  D. J.,, Pascal,  E.,, and Lazarowitz,  S. G.. (1995);  Both bipartite geminivirus movement proteins define viral host range, but only BL1 determines viral pathogenicity.  Virology. 207 191-204
  • 14 Jeske,  H., and Werz,  G.. (1978);  The influence of light intensity on pigment composition and ultrastructure of plastids in leaves of diseased Abutilon sellowianum Reg. (Malvaceae).  Phytopath. Z.. 91 1-13
  • 15 Jorgensen,  R. A.,, Atkinson,  R. G.,, Forster,  R. L. S.,, and Lucas,  W. J.. (1998);  An RNA-based information superhighway in plants.  Science. 279 1486-1487
  • 16 Koch,  K.. (1996);  Carbohydrate modulated gene expression in plants.  Annu. Rev. Plant Physiol. Plant. Mol. Biol.. 47 509-540
  • 17 Krapp,  A.,, Hofmann,  B.,, Schäfer,  C.,, and Stitt,  M.. (1993);  Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the “sink regulation” of photosynthesis?.  Plant J.. 3 817-828
  • 18 Krapp,  A., and Stitt,  M.. (1995);  An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold girdling source leaves.  Planta. 195 313-323
  • 19 Lohaus,  G.,, Winter,  H.,, Riens,  B.,, and Heldt,  H. W.. (1995);  Further studies of the phloem loading process in leaves of barley and spinach: comparison of metabolite concentrations in the apoplastic compartment with those in the cytosolic compartment and in the sieve tubes.  Bot. Acta. 103 270-275
  • 20 Lucas,  W. L.,, Balachandran,  S.,, Park,  J.,, and Wolf,  S.. (1996);  Plasmodesmal companion cell-mesophyll communication in the control over carbon metabolism and phloem transport: insights gained from viral movement proteins.  J. Expt. Bot.. 47 1119-1128
  • 21 Lucas,  W. L., and Gilbertson,  R. L.. (1994);  Plasmadesmata in relation to viral movement in leaf tissues.  Ann. Rev. Phytopathol.. 32 387-411
  • 22 Maxwell,  D. P.,, Laudenbach,  D. E.,, and Huner,  N. P. A.. (1995);  Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. .  Plant Physiol.. 109 787-795
  • 23 Osmond,  C. B.,, Daley,  P. F.,, Badger,  M. R.,, and Lüttge,  U.. (1998);  Chlorophyll fluorescence quenching during photosynthetic induction in leaves of Abutilon striatum Dicks. infected with Abutilon mosaic virus, observed with a field-portable imaging system.  Bot. Acta. 111 390-397
  • 24 Rolfe,  S. A., and Scholes,  J. D.. (1995);  Quantitative imaging of chlorophyll fluorescence.  New Phytol.. 131 69-79
  • 25 Scholes,  J. D.,, Lee,  P. J.,, Horton,  P.,, and Lewis,  D. H.. (1994);  Invertase; understanding changes in the photosynthetic and carbohydrate metabolism of barley leaves infected with powdery mildew.  New Phytol.. 126 213-222
  • 26 Scholes,  J. D., and Rolfe,  S. A.. (1996);  Photosynthesis in localized regions of oat leaves infected with crown rust (Puccinia coronata): quantitative imaging of chlorophyll fluorescence.  Planta. 199 573-582
  • 27 Schuchalter-Eicke,  G., and Jeske,  H.. (1983);  Seasonal changes in the chloroplast ultrastructure in Abutilon mosaic virus (AbMV) infected Abutilon spec. (Malvaceae).  Phytopath. Z.. 108 172-184
  • 28 Siebke,  K., and Weis,  E.. (1995);  Imaging of chlorophyll-a-fluorescence in leaves: topography of photosynthetic oscillations in leaves of Glechoma hederacea. .  Photosyn. Res.. 45 225-237
  • 29 Técsi,  L. I.,, Smith,  A. M.,, Manle,  A. J.,, and Leegood,  R. C.. (1996);  A spatial analysis of physiological changes associated with infection of cotyledons of marrow plants with cucumber mosaic virus.  Plant Physiol.. 111 975-985
  • 30 van Kooten,  O., and Snel,  J. F. H.. (1990);  The use of fluorescence nomenclature in plant stress physiology.  Photosynth. Res.. 25 147-150
  • 31 Wege,  C.. (1998) Gewebespezifische und subzelluläre Verteilungsmuster von DNA und Protein eng verwandter Geminiviren in systemisch infizierter Wirtspflanzen. Thesis, Biologisches Institut, Universität Stuttgart; Ulrich E. Grauer Verlag, Stuttgart

C. B. Osmond

Photobioenergetics Group Research School of Biological Sciences Institute of Advanced Studies The Australian National University

Box 3252

Weston Creek ACT 2611

Australia

Section Editor: U. Lüttge

Email: osmond@rsbs.anu.edu.au

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