Annals of Forest Science

, 76:119 | Cite as

Increased tolerance to Phytophthora cinnamomi in offspring of ink-diseased chestnut (Castanea sativa Miller) trees

  • Álvaro Camisón
  • M. Ángela Martín
  • Jonàs Oliva
  • Malin Elfstrand
  • Alejandro SollaEmail author
Research Paper


Key message

Increased tolerance to Phytophthora cinnamomi was observed in small-sized offspring of ink-diseased chestnut trees, suggesting that a virulent pathogen can trigger a defence response of trees in the subsequent generation. Increased tolerance to water stress was not observed in offspring of chestnut trees.


In sweet chestnut (Castanea sativa Miller), P. cinnamomi Rands is responsible for the widespread and destructive ink disease.


We investigated if the susceptibility of C. sativa to water stress and P. cinnamomi depends on the health status of mother trees.


Plants were grown from seeds collected from healthy and ink-diseased chestnut trees. Leaf wilting after drought exposure and plant mortality after pathogen inoculation were assessed.


Offspring of ink-diseased trees had poorer performance in plant height and root biomass than offspring of healthy trees, with allocation of biomass to seeds mediating this effect. Leaf wilting due to water stress was similar in offspring of healthy and P. cinnamomi-infected trees. However, increased tolerance to P. cinnamomi was observed in small-sized seedlings, suggesting that tolerance in C. sativa may involve growth costs. This is the first report of increased tolerance to P. cinnamomi in plants germinating from a diseased tree.


The results suggest that an invasive pathogen can regulate the performance and prime a defence response of a forest tree species in the subsequent generation, and generate conflicting selection pressures related to plant size.


Tree regeneration Maternal effects Invasive pathogen Priming Stress memory 



The authors are grateful to José Miguel Sillero and Ester Vega for assistance during field sampling, Francisco de Dios, Francisco Javier Dorado and Francisco Alcaide for technical assistance during plant assessment, and Jane McGrath for English editing of the manuscript. They also thank Dr. Santiago Catalá and Dr. Paloma Abad-Campos (Polytechnic University of Valencia) for soil sampling and confirming the presence/absence of Phytophthora cinnamomi under the chestnut trees, and Dr. Susana Serrazina, Dr. Rita Costa and Dr. Carmen Santos for the help in selecting the study genes.


This work was funded by the Spanish Ministry of Economy and Competitiveness [AGL2014-53822-C2-1-R] and the European Union’s European Regional Development Fund (ERDF) ‘A way to achieve Europe’ and the Government of Extremadura (Ref. GR18193). MAM Martín is grateful to the Secretaría General de Ciencia, Tecnología e Innovación, Regional Government of Extremadura (Spain), for financial assistance (‘Atracción de Talento Investigador’ Programme). JO was supported by a ‘Ramon y Cajal’ fellowship (RYC-2015-17459).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. Alcaide F, Solla A, Mattioni C, Castellana S, Martín MÁ (2019) Adaptive diversity and drought tolerance in Castanea sativa assessed through EST-SSR genic markers. Forestry 92:287–296Google Scholar
  2. Ashraf MA, Akbar A, Askari SH, Iqbal M, Rasheed R, Hussain I (2018) Recent advances in abiotic stress tolerance of plants through chemical priming: an overview. In: Rakshit A, Singh HB (eds) Advances in seed priming. Springer, Singapore, pp 51–79Google Scholar
  3. Avramova Z (2019) Defence-related priming and responses to recurring drought: two manifestations of plant transcriptional memory mediated by the ABA and JA signalling pathways. Plant Cell Environ 42:983–997PubMedGoogle Scholar
  4. Alcaide F, Solla A, Cherubini M, Mattioni C, Cuenca B, Camisón Á, Martín MÁ (2020) Adaptive evolution of chestnut forests to the impact of ink disease in Spain. J Syst Evol 58 doi: 10.1111/jse.12551Google Scholar
  5. Bahuguna RN, Tamilselvan A, Muthurajan R, Solis CA, Jagadish SVK (2018) Mild preflowering drought priming improves stress defences, assimilation and sink strength in rice under severe terminal drought. Funct Plant Biol 45:827–839Google Scholar
  6. Camisón Á, Miguel R, Marcos JL, Revilla J, Tardáguila MÁ, Hernández D, Lakicevic M, Jovellar LC, Silla F (2015) Regeneration dynamics of Quercus pyrenaica Willd. in the Central System (Spain). For Ecol Manag 343:42–52Google Scholar
  7. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Report 11:113–116Google Scholar
  8. Ciordia M, Feito I, Pereira-Lorenzo S, Fernández A, Majada J (2012) Adaptive diversity in Castanea sativa Mill. half-sib progenies in response to drought stress. Environ Exp Bot 78:56–63Google Scholar
  9. Conedera M, Tinner W, Krebs P, de Rigo D, Caudullo G (2016) Castanea sativa in Europe: distribution, habitat, usage and threats. In: San-Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A (eds) European atlas of forest tree species. Publ. Off. EU, Luxembourg, pp 78–79Google Scholar
  10. Corcobado T, Solla A, Madeira MA, Moreno G (2013) Combined effects of soil properties and Phytophthora cinnamomi infections on Quercus ilex decline. Plant Soil 373:403–413Google Scholar
  11. Corcobado T, Miranda-Torres JJ, Martín-García J, Jung T, Solla A (2017) Early survival of Quercus ilex subspecies from different populations after infections and co-infections by multiple Phytophthora species. Plant Pathol 66:792–804Google Scholar
  12. Cubera E, Moreno G, Solla A, Madeira M (2012) Root system of Quercus suber L. seedlings in response to herbaceous competition and different watering and fertilisation regimes. Agrofor Syst 85:205–214Google Scholar
  13. Cuestas MI, Mattioni C, Martín LM, Vargas-Osuna E, Cherubini M, Martín MA (2017) Functional genetic diversity of chestnut (Castanea sativa Mill.) populations from southern Spain. For Syst 26:eSC06Google Scholar
  14. Camisón A, Martín MÁ, Sánchez-Bel P, Flors V, Alcaide F, Morcuende D, Pinto G, Solla A (2019) Hormone and secondary metabolite profiling in chestnut during susceptible and resistant interactions with Phytophthora cinnamomi. J Plant Physiol 241:153030PubMedGoogle Scholar
  15. Camisón A, Martín MÁ, Dorado FJ, Moreno G, Solla A (2020) Changes in carbohydrates induced by drought and waterlogging in Castanea sativa. Trees doi: 10.1007/s00468-019-01939-xGoogle Scholar
  16. Çiçek E, Tilki F (2007) Seed size effects on germination, survival and seedling growth of Castanea sativa Mill. J Biol Sci 7:438–441Google Scholar
  17. D’Urso A, Brickner JH (2017) Epigenetic transcriptional memory. Curr Genet 63:435–439PubMedGoogle Scholar
  18. Dewan S, Vander Mijnsbrugge K, De Frenne P, Steenackers M, Michiels B, Verheyen K (2018) Maternal temperature during seed maturation affects seed germination and timing of bud set in seedlings of European black poplar. For Ecol Manag 410:126–135Google Scholar
  19. Dinis LT, Peixoto F, Zhang C, Martins L, Costa R, Gomes-Laranjo J (2011) Physiological and biochemical changes in resistant and sensitive chestnut (Castanea) plantlets after inoculation with Phytophthora cinnamomi. Physiol Mol Plant Pathol 75:146–156Google Scholar
  20. Ferrenberg S, Kane JM, Langenhan JM (2015) To grow or defend? Pine seedlings grow less but induce more defences when a key resource is limited. Tree Physiol 35:107–111PubMedGoogle Scholar
  21. Gonthier P, Nicolotti G (Eds.) (2013). Infectious forest diseases. Cabi, Oxfordshire, UKGoogle Scholar
  22. Ho DH (2014) Transgenerational epigenetics: the role of maternal effects in cardiovascular development. Integr Comp Biol 54:43–51PubMedPubMedCentralGoogle Scholar
  23. Jung T, Blaschke H, Neumann P (1996) Isolation, identification and pathogenicity of Phytophthora species from declining oak stands. Eur J For Pathol 26:253–272Google Scholar
  24. Jung T, Pérez-Sierra A, Durán A, Jung MH, Balci Y, Scanu B (2018) Canker and decline diseases caused by soil-and airborne Phytophthora species in forests and woodlands. Persoonia 40:182–220PubMedPubMedCentralGoogle Scholar
  25. Kassambara A, Kosinski M (2017) Survminer: drawing survival curves using ‘ggplot2’. R Package Version R Foundation for Statistical Computing, Vienna, Austria.
  26. Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60PubMedPubMedCentralGoogle Scholar
  27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆Ct method. Methods 25:402–408Google Scholar
  28. Lopez-Iglesias B, Villar R, Poorter L (2014) Functional traits predict drought performance and distribution of Mediterranean woody species. Acta Oecol 56:10–18Google Scholar
  29. Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963Google Scholar
  30. Martin MA, Mattioni C, Cherubini M, Taurchini D, Villani F (2010) Genetic diversity in European chestnut populations by means of genomic and genic microsatellite markers. Tree Genet Genomes 6:735–744Google Scholar
  31. Martín MA, Monedero E, Martín LM (2017) Genetic monitoring of traditional chestnut orchards reveals a complex genetic structure. Ann For Sci 74:15Google Scholar
  32. Martín-García J, Solla A, Corcobado T, Siasou E, Woodward S (2015) Influence of temperature on germination of Quercus ilex in Phytophthora cinnamomi, P. gonapodyides, P. quercina and P. psychrophila infested soils. For Pathol 45:215–223Google Scholar
  33. Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68:485–512PubMedGoogle Scholar
  34. Maurel M, Robin C, Capdevielle X, Loustau D, Desprez-Loustau ML (2001) Effects of variable root damage caused by Phytophthora cinnamomi on water relations of chestnut saplings. Ann For Sci 58:639–651Google Scholar
  35. Mora-Sala B, Berbegal M, Abad-Campos P (2018) The use of qPCR reveals a high frequency of Phytophthora quercina in two Spanish holm oak areas. Forests 9:697Google Scholar
  36. Moreira X, Zas R, Solla A, Sampedro L (2015) Differentiation of persistent anatomical defensive structures is costly and determined by nutrient availability and genetic growth-defence constraints. Tree Physiol 35:112–123PubMedGoogle Scholar
  37. Osswald W, Fleischmann F, Rigling D et al (2014) Strategies of attack and defence in woody plant–Phytophthora interactions. For Pathol 44:169–190Google Scholar
  38. Phillips DH, Burdekin DA (1982) Diseases of sweet chestnut (Castanea spp.). In: Phillips DH, Burdekin DA (eds) Diseases of forest and ornamental trees. Palgrave Macmillan, London, pp. 273–283Google Scholar
  39. Pliura A, Eriksson G (2002) Genetic variation in juvenile height and biomass of open-pollinated families of six Castanea sativa Mill. populations in a 2 x 2 factorial temperature x watering experiment. Silvae Genet 51:152–160Google Scholar
  40. Pazianoto LHR, Solla A, Ferreira V (2019) Leaf litter decomposition of sweet chestnut is affected more by oomycte infection of trees than by water temperature. Fungal Ecol 41:269–278Google Scholar
  41. Ramírez-Valiente JA, Valladares F, Gil L, Aranda I (2009) Population differences in juvenile survival under increasing drought are mediated by seed size in cork oak (Quercus suber L.). For Ecol Manag 257:1676–1683Google Scholar
  42. Redondo MÁ, Pérez-Sierra A, Abad-Campos P, Torres L, Solla A, Reig-Armiñana J, García-Breijo F (2015) Histology of Quercus ilex roots during infection by Phytophthora cinnamomi. Trees 29:1943–1957Google Scholar
  43. Robin C, Morel O, Vettraino AM, Perlerou C, Diamandis S, Vannini A (2006) Genetic variation in susceptibility to Phytophthora cambivora in European chestnut (Castanea sativa). For Ecol Manag 226:199–207Google Scholar
  44. Santos C, Machado H, Correia I, Gomes F, Gomes-Laranjo J, Costa R (2015) Phenotyping Castanea hybrids for Phytophthora cinnamomi resistance. Plant Pathol 64:901–910Google Scholar
  45. Santos C, Duarte S, Tedesco S, Fevereiro P, Costa RL (2017) Expression profiling of Castanea genes during resistant and susceptible interactions with the oomycete pathogen Phytophthora cinnamomi reveal possible mechanisms of immunity. Front Plant Sci 8:515PubMedPubMedCentralGoogle Scholar
  46. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671PubMedPubMedCentralGoogle Scholar
  47. Serrazina S, Santos C, Machado H, Pesquita C, Vicentini R, Pais MS, Sebastiana M, Costa R (2015) Castanea root transcriptome in response to Phytophthora cinnamomi challenge. Tree Genet Genomes 11:1–19Google Scholar
  48. Shi W, Villar-Salvador P, Li G, Jiang X (2019) Acorn size is more important than nursery fertilization for outplanting performance of Quercus variabilis container seedlings. Ann For Sci 76:22Google Scholar
  49. Silla F, Camisón A, Solana A, Hernández H, Ríos G, Cabrera M, López D, Morera A (2018) Does the persistence of sweet chestnut depend on cultural inputs? Regeneration, recruitment, and mortality in Quercus- and Castanea-dominated forests. Ann For Sci 75:95Google Scholar
  50. Solla A, Aguín O, Cubera E, Sampedro L, Mansilla JP, Zas R (2011) Survival time analysis of Pinus pinaster inoculated with Armillaria ostoyae: genetic variation and relevance of seed and root traits. Eur J Plant Pathol 130:477–488Google Scholar
  51. Soylu A, Eris A, Özgür M, Dalkiliç Z (1999) Researches on the rootstock potentiality of chestnut types (Castanea sativa Mill.) grown in Marmara region. Acta Hortic 494:213–222Google Scholar
  52. Therneau T (2015) A package for survival analysis in S. version 2.38Google Scholar
  53. Uller T, Nakagawa S, English S (2013) Weak evidence for anticipatory parental effects in plants and animals. J Evol Biol 26:2161–2170PubMedGoogle Scholar
  54. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40(15):e115PubMedPubMedCentralGoogle Scholar
  55. Vettraino AM, Morel O, Perlerou C, Robin C, Diamandis S, Vannini A (2005) Occurrence and distribution of Phytophthora species in European chestnut stands, and their association with ink disease and crown decline. Eur J Plant Pathol 111:169–180Google Scholar
  56. Villar-Salvador P, Peñuelas JL, Jacobs DF (2012) Nitrogen nutrition and drought hardening exert opposite effects on the stress tolerance of Pinus pinea L. seedlings. Tree Physiol 33:221–232Google Scholar
  57. Vivas M, Zas R, Sampedro L, Solla A (2013) Environmental maternal effects mediate the resistance of maritime pine to biotic stress. PLoS One 8:e70148PubMedPubMedCentralGoogle Scholar
  58. Vivas M, Nunes C, Coimbra MA, Solla A (2014a) Antioxidant activity of Pinus pinaster infected with Fusarium circinatum is influenced by maternal effects. Forest Pathol 44:337–340Google Scholar
  59. Vivas M, Nunes C, Coimbra MA, Solla A (2014b) Maternal effects and carbohydrate changes of Pinus pinaster after inoculation with Fusarium circinatum. Trees 28:373–379Google Scholar
  60. Vivas M, Rolo V, Wingfield MJ, Slippers B (2019) Maternal environment regulates morphological and physiological traits in Eucalyptus grandis. For Ecol Manag 432:631–636Google Scholar
  61. Wang X, Zhang X, Chen J, Wang X, Cai J, Zhou Q, Dai T, Cao W, Jiang D (2018) Parental drought-priming enhances tolerance to post-anthesis drought in offspring of wheat. Front Plant Sci 9:261PubMedPubMedCentralGoogle Scholar
  62. Younginger BS, Sirová D, Cruzan MB, Ballhorn DJ (2017) Is biomass a reliable estimate of plant fitness? Appl Plant Sci 5:1600094Google Scholar
  63. Zas R, Cendán C, Sampedro L (2013) Mediation of seed provisioning in the transmission of environmental maternal effects in maritime pine (Pinus pinaster Aiton). Heredity 111:248–255PubMedPubMedCentralGoogle Scholar
  64. Zhang Z (2016) Semi-parametric regression model for survival data: graphical visualization with R. Ann Transl Med 4:461PubMedPubMedCentralGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute for Dehesa Research (INDEHESA), Faculty of ForestryUniversity of ExtremaduraPlasenciaSpain
  2. 2.Escuela Técnica Superior de Ingeniería Agronómica y de Montes, Departamento de Genética, Edificio Gregor Mendel, Campus de RabanalesUniversidad de CórdobaCórdobaSpain
  3. 3.Department of Crop and Forest SciencesUniversity of LleidaLleidaSpain
  4. 4.Joint Research UnitAgrotecnio-CTFCLleidaSpain
  5. 5.Biocentrum, Department of Forest Mycology and Plant PathologySwedish University of Agricultural Sciences (SLU)UppsalaSweden

Personalised recommendations