Skip to main content

Advertisement

Springer Nature Link
Log in

Damage response involves mechanisms conserved across plants, animals and fungi

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

All organisms are constantly exposed to adverse environmental conditions including mechanical damage, which may alter various physiological aspects of growth, development and reproduction. In plant and animal systems, the damage response mechanism has been widely studied. Both systems posses a conserved and sophisticated mechanism that in general is aimed at repairing and preventing future damage, and causes dramatic changes in their transcriptomes, proteomes, and metabolomes. These damage-induced changes are mediated by elaborate signaling networks, which include receptors/sensors, calcium (Ca2+) influx, ATP release, kinase cascades, reactive oxygen species (ROS), and oxylipin signaling pathways. In contrast, our current knowledge of how fungi respond to injury is limited, even though various reports indicate that mechanical damage triggers reproductive processes. In fungi, the damage response mechanism has been studied more in depth in Trichoderma atroviride. Interestingly, these studies indicate that the mechanical damage response involves ROS, Ca2+, kinase cascades, and lipid signaling pathways. Here we compare the response to mechanical damage in plants, animals and fungi and provide evidence that they appear to share signaling molecules and pathways, suggesting evolutionary conservation across the three kingdoms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

ROS:

Reactive oxygen species

FIS:

Fruiting inducing substances

Nox:

NADPH oxidase

MAPK:

Mitogen-activated protein kinase

JA:

Jasmonic acid

EGTA:

Ethylene glycol tetraacetic acid (extracellular Ca2+ chelating agent)

PRR:

Pattern recognition receptors

PAMP:

Pathogen-associated molecular patterns

DAMP:

Damage-associated molecular patterns

eATP:

Extracellular ATP

PGE:

Prostaglandins

PO:

Phenoloxidase

JNK:

c-Jun N-terminal kinase

WB:

Woronin body

SO:

SOFT protein

CDPK:

Calcium-dependent protein kinases

CAMK:

Ca2+/calmodulin-dependent kinase

CRZ:

Calcineurin-responsive zinc finger transcription factor

H2O2 :

Hydrogen peroxide

SIPK:

Salicylic acid-induced protein kinase

WIPK:

Wound-induced protein kinase

ERK:

Extracellular signal-regulated kinase

MeJA:

Methyl jasmonate

PCD:

Programed cell death

α-Dox:

α-Dioxygenase

References

  • Aguirre J, Lambeth DJ (2010) Nox enzymes from fungus to fly to fish and what they tell us about Nox function in mammals. Free Radic Biol Med 49:1342–1353. doi:10.1016/j.freeradbiomed.2010.07.027

  • Aguirre J, Rodríguez R, Hansberg W (1989) Oxidation of Neurospora crassa NADP-specific glutamate dehydrogenase by activated oxygen species. J Bacteriol 171(11):6243–6250 (pii 0021-9193/89/116243-08)

  • Aguirre J, Rios-Momberg M, Hewitt D, Hansberg W (2005) Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol 13(3):111–118. doi:10.1016/j.tim.2005.01.007

  • Aguirre J, Hansberg W, Navarro R (2006) Fungal responses to reactive oxygen species. Med Mycol 44:5101–5107. doi:10.1080/13693780600900080

    Google Scholar 

  • Arimura GI, Maffei ME (2010) Calcium and secondary CPK signaling in plants in response to herbivore attack. Biochem Biophys Res Commun 400:455–460. doi:10.1016/j.bbrc.2010.08.134

    CAS  PubMed  Google Scholar 

  • Arimura GI, Ozawa R, Maffei ME (2011) Recent Advances in plant early signaling in response to herbivory. Int J Mol Sci 12:3723–3739. doi:10.3390/ijms12063723

    CAS  PubMed Central  PubMed  Google Scholar 

  • Asai S, Ohta K, Yoshioka H (2008) MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20(5):1390–1406. doi:10.1105/tpc.107.055855

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bachstetter AD, Rowe RK, Kaneko M, Goulding D, Lifshitz J, Van Eldik LJ (2013) The p38α MAPK regulates microglial responsiveness to diffuse traumatic brain injury. J Neurosci 33(14):6143–6153. doi:10.1523/JNEUROSCI.5399-12.2013

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bahn YS, Xue C, Idnurm A, Rutherford JC, Heitman J, Cardenas ME (2007) Sensing the environment: lessons from fungi. Nat Rev Microbiol 5(1):57–69. doi:10.1038/nrmicro1578

    CAS  PubMed  Google Scholar 

  • Bement WM, Mandato CA, Kirsch MN (1999) Wound-induced assembly and closure of an actomyosin purse string in Xenopus oocytes. Curr Biol 9(11):579–587. doi:10.1016/S0960-9822(99)80261-9

  • Bostock RM, Stermer BA (1989) Perspective on wound-healing in resistance to pathogens. Annu Rev Phytopathol 27:343–371. doi:10.1146/annurev.py.27.090189.002015

    Google Scholar 

  • Braam J (1992) Regulation of expression of calmodulin and calmodulin-related genes by environmental stimuli in plants. Cell Calcium 13:457–463. doi:10.1016/0143-4160(92)90058-Z

    CAS  PubMed  Google Scholar 

  • Casas-Flores S, Rios-Momberg M, Bibbins M, Ponce-Noyola P, Herrera-Estrella A (2004) BLR-1 and BLR-2 are key regulatory elements for photoconidiation and mycelial grown in T. atroviride. Microbiology 150:3561–3569. doi:10.1099/mic.0.27346-0

    CAS  PubMed  Google Scholar 

  • Chang C, Wu P, Baker RE, Maini PK, Alibardi L, Chuong CM (2009) Reptile scale paradigm: Evo-Devo, pattern formation and regeneration. Int J Dev Biol 53(5–6):813–826. doi:10.1387/ijdb.072556cc

    PubMed Central  PubMed  Google Scholar 

  • Chang MC, Chen YJ, Lee MY, Lin LD, Wang TM, Chan CP, Tsai YL, Wang CY, Lin BR, Jeng JH (2010) Prostaglandin F2a stimulates MEK/ERK signaling but decreases the expression of alkaline phosphatase in dental pulp cells. Int Endod J 43:461–468. doi:10.1111/j.1365-2591.2010.01699.x

    CAS  PubMed  Google Scholar 

  • Chauhan N, Latge JP, Calderone R (2006) Signalling and oxidant adaptation in Candida albicans and Aspergillus fumigatus. Nat Rev Microbiol 4:435–444. doi:10.1038/nrmicro1426

    CAS  PubMed  Google Scholar 

  • Chen GY, Nuñez G (2010) Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 10:826–837. doi:10.1038/nri2873

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clark AG, Miller AL, Vaughan E, Yu HYE, Penkert R, Bement WM (2009) Integration of single and multicellular wound responses. Curr Biol 19(16):1389–1395. doi:10.1016/j.cub.2009.06.044

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cole GT (1986) Models of cell differentiation in conidial fungi. Microbiol Rev 50(2):95–132 (PMCID: PMC373060)

  • Crosby LM, Waters CM (2010) Epithelial repair mechanisms in the lung. Am J Physiol Lung Cell Mol Physiol 298:715–731. doi:10.1152/ajplung.00361.2009

    Google Scholar 

  • Curach NC, Te’o Valentino SJ, Gibbs MD, Bergquist PL, Nevalainen KMH (2004) Isolation, characterization and expression of the hex1 gene from Trichoderma reesei. Gene 331:133–140. doi:10.1016/j.gene.2004.02.007

    CAS  PubMed  Google Scholar 

  • Das DK, Maulik N (2004) Conversion of death signal into survival signal by redox signaling. Biochemistry (Mosc) 69(1):16–24. doi:10.1023/B:BIRY.0000016345.19027.54

    Google Scholar 

  • De Oliveira S, López-Muñoz A, Candel S, Pelegrín P, Calado A, Mulero V (2014) ATP modulates acute inflammation in vivo through dual oxidase 1-derived H2O2 production and NF-κB activation. J Immunol 192:5710–5719. doi:10.4049/jimmunol.1302902

    PubMed  Google Scholar 

  • Delgado-Jarana J, Sousa S, González F, Rey M, Llobell A (2006) The Hog1 controls the hyperosmotic stress response in Trichoderma harzianum. Microbiology 152:1687–1700. doi:10.1099/mic.0.28729-0

    CAS  PubMed  Google Scholar 

  • Dhondt S, Geoffroy P, Stelmach BA, Legrand M, Heitz T (2000) Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatin-like enzymes. Plant J 23:431–440. doi:10.1046/j.1365-313x.2000.00802.x

    CAS  PubMed  Google Scholar 

  • Dombrowski JE, Hind SR, Martin RC, Stratmann JW (2011) Wounding systemically activates a mitogen-activated protein kinase in forage and turf grasses. Plant Sci 180:686–693. doi:10.1016/j.plantsci.2011.01.010

    CAS  PubMed  Google Scholar 

  • Farmer EE, Alméras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6(4):372–378. doi:10.1016/S1369-5266(03)00045-1

    CAS  PubMed  Google Scholar 

  • Fester T, Hause G (2005) Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15:373–379. doi:10.1007/s00572-005-0363-4

    CAS  PubMed  Google Scholar 

  • Fleiβner A, Glass NL (2007) SO, a protein involved in hyphal fusion in Neurospora crassa, localizes to septal plugs. Eukaryot cell 6(1):84–94. doi:10.1128/EC.00268-06

    Google Scholar 

  • Gailit J, Clark RA (1994) Wound repair in the context of extracellular matrix. Curr Opin Cell Biol 6(5):717–725. doi:10.1016/0955-0674(94)90099-X

    CAS  PubMed  Google Scholar 

  • Gfeller A, Liechti R, Farmer EE (2010) Arabidopsis jasmonate signaling pathway. Sci Signal 3(109):cm4. doi:10.1126/scisignal.3109cm4

  • Gfeller A, Baerenfaller K, Loscos J, Chételat A, Baginsky S, Farmer EE (2011) Jasmonate controls polypeptide patterning in undamaged tissue in wounded Arabidopsis leaves. Plant Physiol 156(4):1797–1807. doi:10.1104/pp.111.181008

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gurtner GC, Werner S, Barrandon Y, Longaker MT (2008) Wound repair and regeneration. Nature 453(7193):314–321. doi:10.1038/nature07039

    CAS  PubMed  Google Scholar 

  • Hagiwara D, Mizuno T, Abe K (2009) Characterization of NikA histidine kinase and two response regulators with special reference to osmotic adaptation and asexual development in Aspergillus nidulans. Biosci Biotechnol Biochem 73(7):1566–1571. doi:10.1271/bbb.90063

  • Hegedüs N, Sigl C, Zadra I, Pócsi I, Marx F (2011) The paf gene product modulates asexual development in Penicillium chrysogenum. J Basic Microbiol 51:253–262. doi:10.1002/jobm.201000321

    PubMed Central  PubMed  Google Scholar 

  • Heil M (2009) Damaged-self recognition in plant herbivore defense. Trends Plant Sci 14:356–363. doi:10.1016/j.tplants.2009.04.002

    CAS  PubMed  Google Scholar 

  • Heil M (2012) Damaged-self recognition as a general strategy for injury detection. Plant Signal Behav 7(5):576–580. doi:10.4161/psb.19921

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heil M, Ibarra-Laclette E, Adame-Álvarez RM, Martínez O, Ramirez-Chávez E, Molina- Torres J, Herrera-Estrella L (2012) How plants sense wounds: damaged-self recognition is based on plant-derived elicitors and induces octadecanoid signaling. PLoS One 7:e30357. doi:10.1371/journal.pone.0030537

    Google Scholar 

  • Henis Y, Chet I, Avizohar-Hershenzon Z (1965) Nutritional and mechanical factors involved in mycelial growth and production of Sclerotial by Sclerotium rolfsii in artificial medium and amended soil. Phytopathol 55:87–91

    CAS  Google Scholar 

  • Hernández-Oñate MA, Esquivel-Naranjo EU, Mendoza-Mendoza A, Stewart A, Herrera- Estrella AH (2012) An injury-response mechanism conserved across kingdoms determines entry of the fungus Trichoderma atroviride into development. Proc Natl Acad Sci USA 109:14918–14923. doi:10.1073/pnas.1209396109

    PubMed Central  PubMed  Google Scholar 

  • Jaffe LF (2010) Fast calcium waves. Cell Calcium 48:102–113. doi:10.1016/j.ceca.2010.08.007

    CAS  PubMed  Google Scholar 

  • Jang HS, Han SJ, Kim JI, Lee S, Lipschutz JH, Park KM (2013) Activation of ERK accelerates repair of renal tubular epithelial cells, whereas it inhibits progression of fibrosis following ischemia/reperfusion injury. Biochim Biophys Acta Mol Basis Dis 1832:1998–2008. doi:10.1016/j.bbadis.2013.07.001

    CAS  Google Scholar 

  • Jedd G (2011) Fungal evo-devo: organelles and multicellular complexity. Trends Cell Biol 21(1):12–19. doi:10.1016/j.tcb.2010.09.001

    CAS  PubMed  Google Scholar 

  • Jedd G, Chua N-H (2000) A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat Cell Biol 2:226–231. doi:10.1038/35008652

    CAS  PubMed  Google Scholar 

  • Jendretzki A, Winttland J, Wilk S, Straede A, Heinisch JJ (2011) How do I begin? Sensing extracellular stress to maintain yeast cell wall integrity. Eur J Cell Biol 90(9):740–744. doi:10.1016/j.ejcb.2011.04.006

    CAS  PubMed  Google Scholar 

  • Jiang F, Zhang Y, Dusting GJ (2011) NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol Rev 63(1):218–242. doi:10.1124/pr.110.002980

    CAS  PubMed  Google Scholar 

  • Juvvadi PR, Maruyama JI, Kitamoto K (2007) Phosphorilation of the Aspergillus oryzae Woronin body protein, AoHex1, by protein kinase C: evidence for its role in the multimerization and proper localization of the Woronin body protein. Biochem J 405:533–540. doi:10.1042/BJ20061678

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kandoth PK, Ranf S, Pancholi SS, Jayanty S, Walla MD, Miller W, Howe GA, Lincoln DE, Stratmann JW (2007) Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects. Proc Natl Acad Sci USA 104(29):12205–12210. doi:10.1073/pnas.0700344104

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kawate T, Michel JC, Birdsong WT, Gouaux E (2009) Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 460:592–598. doi:10.1038/nature08198

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim M, McGinnis W (2011) Phosphorylation of grainy head by ERK is essential for wound-dependent regeneration but not for development of an epidermal barrier. Proc Natl Acad Sci USA 108:650–655. doi:10.1073/pnas.1016386108

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim CY, Liu Y, Thorne ET, Yang H, Fukushige H, Gassmann W, Hildebrand D, Sharp RE, Zhang S (2003) Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell 15:2707–2718. doi:10.1105/tpc.011411

  • Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19(3):1065–1080. doi:10.1105/tpc.106.048884

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koo AJK, Howe GA (2009) The wound hormone jasmonate. Phytochem 70(13–14):1571–1580. doi:10.1016/j.phytochem.2009.07.018

    CAS  Google Scholar 

  • Koo AJ, Gao X, Daniel Jones A, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59(6):974–986. doi:10.1111/j.1365-313X.2009.03924.x

    CAS  PubMed  Google Scholar 

  • Kurashima Y, Amiya T, Nochi T, Fujisawa K, Haraguchi T, Iba H, Tsutsui H, Sato S, Nakajima S, Iijima H, Kubo M, Kunisawa J, Kiyono H (2012) Extracellular ATP mediates mast cell-dependent intestinal inflammation through P2X7 purinoceptors. Nat Commun 3:1034. doi:10.1038/ncomms2023

    PubMed Central  PubMed  Google Scholar 

  • Kurusu T, Yagala T, Miyao A, Hirochika H, Kuchitsu K (2005) Identification of a putative voltage-gated Ca2+ channel as a key regulator of elicitor-induced hypersensitive cell death mitogen-activated protein kinase activation in rice. Plant J 42(6):798–809. doi:10.1111/j.1365-313X.2005.02415.x

    CAS  PubMed  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Ann Rev Plant Physiol Plant Mol Biol 48(1):251–275. doi:10.1146/annurev.arplant.48.1.251

    CAS  Google Scholar 

  • Land WG (2013) Transfusion-related acute lung injury: the work of DAMPs. Transfus Med Hemother 40(1):3–13. doi:10.1159/000345688

    PubMed Central  PubMed  Google Scholar 

  • Land WG, Messmer K (2012) The danger theory in view of the injury hypothesis: 20 years later. Front Immunol 3:349. doi:10.3389/fimmu.2012.00349

    PubMed Central  PubMed  Google Scholar 

  • Lara-Rojas F, Sánchez O, Kawasaki L, Aguirre J (2011) Aspergillus nidulans transcription factor AtfA interacts with the MAPK SakA to regulate general stress responses, development spore functions. Mol Microbiol 80(2):436–454. doi:10.1111/j.1365-2958.2011.07581.x

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leiter É, Szappanos H, Oberparleiter C, Kaiserer L, Csernoch L, Pusztahelyi T, Emri T, Pócsi I, Salvenmoser W, Marx F (2005) Antifungal protein PAF severely affects the integrity of the plasma membrane of Aspergillus nidulans induces an apoptosis-like phenotype. Antimicrob Agents Chemother 49(6):2445–2453. doi:10.1128/AAC.49.6.2445-2453.2005

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leitner M, Boland W, Mithöfer A (2005) Direct indirect defences induced by piercing-sucking chewing herbivores in Medicago truncatula. New Phytol 167:597–606. doi:10.1111/j.1469-8137.2005.01426.x

    CAS  PubMed  Google Scholar 

  • León J, Rojo E, Sánchez-Serrano JJ (2001) Wound signaling in plants. J Exp Bot 52(354):1–9. doi:10.1093/jexbot/52.354.1

    PubMed  Google Scholar 

  • Leonard TJ, Dick S (1968) Chemical induction of haploid fruiting bodies in Schizophyllum commune. Proc Natl Acad Sci USA 59:745–751 (PMCID: PMC224738)

  • Leonard TJ, Dick S (1973) Induction of haploid fruiting by mechanical injury in Schizophyllum commune. Mycol 65:809–822. http://www.jstor.org/stable/3758520

  • Leonard TJ, Raper JR (1969) Schizophyllum commune: gene controlling induced haploid fruiting. Science 165:190. doi:10.1126/science.165.3889.190

    CAS  PubMed  Google Scholar 

  • Li M, Guo W, Zhang P, Li H, Gu X, Yao D (2013) Signal flow pathways in response to early Wallerian degeneration after rat sciatic nerve injury. Neurosci Lett 536:56–63. doi:10.1016/j.neulet.2013.01.008

    CAS  PubMed  Google Scholar 

  • Liu F, Ng Kah, Seng LuY, Low W, Lai J, Jedd G (2008) Making two organelles from one: Woronin body biogenesis by peroxisomal protein sorting. J Cell Biol 180(2):325–339. doi:10.1083/jcb.200705049

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu F, Lu Y, Pieuchot L, Dhavale T, Jedd G (2011) Import oligomers induce positive feedback to promote peroxisome differentiation control organelle abundance. Dev Cell 21(3):457–468. doi:10.1016/j.devcel.2011.08.004

    CAS  PubMed  Google Scholar 

  • Lulai EC, Corsini DL (1998) Differential deposition of suberin phenolic aliphatic domains their roles in resistance to infection during potato tuber (Solanum tuberosumL.) wound-healing. Physiol Mol Plant Pathol 53(4):209–222. doi:10.1006/pmpp.1998.0179

    CAS  Google Scholar 

  • Maffei M, Bossi S, Spiteller D, Mithöfer A, Boland W (2004) Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, regurgitate components. Plant Physiol 134(4):1752–1762. doi:10.1104/pp.103.034165

    CAS  PubMed Central  PubMed  Google Scholar 

  • Markham P (1994) Occlusions of septal pores in filamentous fungi. Mycol Res 98(10):1089–1106. doi:10.1016/S0953-7562(09)80195-0

    Google Scholar 

  • Martin P, Leibovich SJ (2005) Inflammatory cells during wound repair: the good, the bad the ugly. Trends Cell Biol 15(11):599–607. doi:10.1016/j.tcb.2005.09.002

    CAS  PubMed  Google Scholar 

  • Maruyama JI, Juvvadi PR, Ishi K, Kitamoto K (2005) Three-dimensional image analysis of plugging at the septal pore by Woronin body during hypotonic shock inducing hyphal tip bursting in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 331:1081–1088. doi:10.1016/j.bbrc.2005.03.233

    CAS  PubMed  Google Scholar 

  • McCord JM (2000) The evolution of free radicals oxidative stress. Am J Med 108(8):652–659. doi:http://dx.doi.org/10.1016/S0002-9343(00)00412-5

  • Medders KE, Kaul M (2011) Mitogen-activated protein kinase p38 in HIV infection associated brain injury. J Neuroimmune Pharmacol 6(2):202–215. doi:10.1007/s11481-011-9260-0

    PubMed Central  PubMed  Google Scholar 

  • Medina-Castellanos E, Esquivel-Naranjo EU, Heil M, Herrera-Estrella A (2014) Extracellular ATP activates MAPK and ROS signaling during injury response in the fungus Trichoderma atroviride. Front Plant Sci 5:659. doi:10.3389/fpls.2014.00659

    PubMed Central  PubMed  Google Scholar 

  • Mendoza-Mendoza A, Pozo MJ, Grzegorski D, Martínez P, García JM, Olmedo-Monfil V, Cortés C, Kenerley C, Herrera-Estrella A (2003) Enhanced biocontrol activity of Trichoderma through inactivation of a mitogen-activated protein kinase. Proc Natl Acad Sci USA 100(26):15965–15970. doi:10.1073/pnas.2136716100

    CAS  PubMed Central  PubMed  Google Scholar 

  • Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shualaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediated rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45. doi:10.1126/scisignal.2000448

    PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Breusegem FV (2011) ROS signaling: the new wave? Trends Plant Sci 16(6):300–309. doi:10.1016/j.tplants.2011.03.007

    CAS  PubMed  Google Scholar 

  • Momany M, Richardson EA, Van Sickle C, Jedd G (2002) Mapping Woronin body position in Aspergillus nidulans. Mycol 94(2):260–266

    Google Scholar 

  • Mosblech A, Feussner I, Heilmann I (2010) Oxylipin signaling plant growth. In: Munnik T (ed) Lipid signaling in plants, series: plant cell monographs, vol 16, pp 277–291. Springer, Berlin

  • Müller WH, Montijn RC, Humbel BM, van Aelst AC, Boon EJ, van der Krift TP, Boekhout T (1998) Structural differences between two types of basidiomycete septal pore caps. Microbiol 144:1721–1730. doi:10.1099/00221287-144-7-1721

    Google Scholar 

  • Nam HJ, Jang IH, You H, Lee KA, Lee WJ (2012) Genetic evidence of a redox-dependent systemic wound response via Hayan protease-phenoloxidase system in Drosophila. EMBO J 31(5):1253–1265. doi:10.1038/emboj.2011.476

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nelson G, Kozlova-Zwinderman O, Collis AJ, Knight MR, Fincham JRS, Stanger CP, Hessing JGM, Punt PJ, van den Hondel CAMJ, Read ND (2004) Calcium measurement in living filamentous fungi expressing codon-optimized aequorin. Mol Microbiol 52(5):1437–1450. doi:10.1111/j.1365-2958.2004.04066.x

    CAS  PubMed  Google Scholar 

  • Noordermeer MA, Veldink GA, Vliegenthart JF (2001) Fatty acid hydroperoxide lyase: a plant cytochrome p450 enzyme involved in wound healing pest resistance. ChemBioChem 2(7–8):494–504. doi:10.1002/1439-7633(20010803)2:7/8<494:AID-CBIC494>3.0.CO;2-1

    CAS  PubMed  Google Scholar 

  • Noverr MC, Erb-Downward JR, Huffnagle GB (2003) Production of eicosanoids other oxylipins by pathogenic eukaryotic microbes. Clin Microbiol Rev 16(3):517–533. doi:10.1128/CMR.16.3.517-533.2003

    CAS  PubMed Central  PubMed  Google Scholar 

  • Orozco-Cardenas M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 96(11):6553–6557. doi:10.1073/pnas.96.11.6553

    CAS  PubMed Central  PubMed  Google Scholar 

  • Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, methyl jasmonate. Plant Cell 13(1):179–191. doi:10.1105/tpc.13.1.179

  • Phillips L, Leonard TJ (1976) Extracellular intracellular phenoloxidase activity during growth development in Schizophyllum. Mycology 68:268–276. http://www.jstor.org/stable/3758998

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12(3):98–105. doi:10.1016/j.tplants.2007.01.004

  • Rämet M, Lanot R, Zachary D, Manfruelli P (2002) JNK signaling pathway is required for efficient wound healing in Drosophila. Dev Biol 241:145–156. doi:10.1006/dbio.2001.0502

    PubMed  Google Scholar 

  • Reithner B, Schuhmacher R, Stoppacher N, Pucher M, Brunner K, Zeilinger S (2007) Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk1 differentially affects mycoparasitism plant protection. Fungal Genet Biol 44:1123–1133. doi:10.1016/j.fgb.2007.04.001

    CAS  PubMed  Google Scholar 

  • Rodríguez-Peña JM, García R, Nombela C, Arroyo J (2010) The high-osmolarity glycerol (HOG) cell wall integrity (CWI) signalling pathways interplay: a yeast dialogue between MAPK routes. Yeast 27(8):495–502. doi:10.1002/yea.1792

    PubMed  Google Scholar 

  • Romeis T, Piedras P, Zhang S, Klessig DF, Hirt H, Jones JD (1999) Rapid Avr9-Cf-9-dependent activation of MAP kinases in tobacco cell cultures leaves: convergence of resistance gene, elicitor, wound, salicylate responses. Plant Cell Online 11(2):273–287. doi:10.1105/tpc.11.2.273

  • Roncal T, Ugalde U (2003) Conidiation induction in Penicillium. Res Microbiol 154:539–546. doi:10.1016/S0923-2508(03)00168-2

    CAS  PubMed  Google Scholar 

  • Rusmin S, Leonard TJ (1978) Biochemical induction of fruiting in Schyzophyllum. Plant Physiol 61:538–543. doi:10.1104/pp.61.4.538

  • Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness development in Lycopersicon esculentum. Plant Cell 16(3):616–628. doi:10.1105/tpc.019398

  • Sasaki H, Yamamoto H, Tominaga K, Masuda K, Kawai T, Teshima-Kondo S, Rokutan K (2009) NADPH oxidase-derived reactive oxygen species are essential for differentiation of a mouse macrophage cell line (RAW264.7) into osteoclasts. J Med Invest 56(1–2):33–41. doi:10.2152/jmi.56.33

  • Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377. doi:10.1016/j.pbi.2005.05.008

    CAS  PubMed  Google Scholar 

  • Seo S, Katou S, Seto H, Gomi K, Ohashi Y (2007) The mitogen-activated protein kinases WIPK SIPK regulate the levels of jasmonic salicylic acids in wounded tobacco plants. Plant J 49(5):899–909. doi:10.1111/j.1365-313X.2006.03003.x

    CAS  PubMed  Google Scholar 

  • Sherwood CL, Lantz RC, Burgess JL, Boitano S (2011) Arsenic alters ATP-dependent Ca2+ signaling in human airway epithelial cell wound response. Toxicol Sci 121:191–206. doi:10.1093/toxsci/kfr044

    CAS  PubMed Central  PubMed  Google Scholar 

  • Steyaert JM, Weld RJ, Mendoza-Mendoza A, Stewart A (2010) Reproduction without sex: conidiation in the filamentous fungus Trichoderma. Microbiology 156:2887–9000. doi:10.1099/mic.0.041715-0

    CAS  PubMed  Google Scholar 

  • Steyaert JM, Weld RJ, Mendoza-Mendoza A, Krystofová S, Simkovic M, Varecka L, Stewart A (2013) Asexual development in Trichoderma: conidia to Chlamydospores. In: Mukherjee P, Horwitz BA, Singh US, Mukherjee M, Schmoll M (eds) Trichoderma: biology and applications. CABI, Oxforshire, pp 87–109

  • Taj G, Agarwal P, Grant M, Kumar A (2010) MAPK machinery in plants: recognition response to different stresses through multiple signal transduction pathways. Plant Signal Behav 5(11):1370–1378. doi:10.4161/psb.5.11.13020

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takemoto D, Tanaka A, Scott B (2006) A p67phox-like regulator is recruited to control hyphal branching in a fugal-grass mutualistic symbiosis. Plant Cell 18:2807–2821. doi:10.1105/tpc.106.046169

  • Takemoto D, Tanaka A, Scott B (2007) NADPH oxidases in fungi: diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet Biol 44:1065–1076. doi:10.1016/j.fgb.2007.04.011

    CAS  PubMed  Google Scholar 

  • Takemoto D, Kamakura S, Saikia S, Becker Y, Wrenn R, Tanaka A, Sumimoto H, Scott B (2011) Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex. Proc Natl Acad Sci USA 108(7):2861–2866. doi:10.1073/pnas.1017309108

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takeuchi O, Akira S (2010) Pattern recognition receptors inflammation. Cell 140:805–820. doi:10.1016/j.cell.2010.01.022

    CAS  PubMed  Google Scholar 

  • Tenney K, Hunt I, Sweigard J, Pounder IJ, McClain C, Bowman JE, Bowman JB (2000) Hex-1, a gene unique to filamentous fungi, encodes the major protein of the Woronin body functions as a plug for septal pores. Fungal Genet Biol 31:205–217. doi:10.1006/fgbi.2000.1230

    CAS  PubMed  Google Scholar 

  • Tey WK, North AJ, Lu YF, Jedd G (2005) Polarized gene expression determines Woronin body formation at the leading edge of the fungal colony. Mol Biol Cell 16(6):2651–2659. doi:10.1091/mbc.E04-10-0937

    CAS  PubMed Central  PubMed  Google Scholar 

  • Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99(1):517–522. doi:10.1073/pnas.012452499

    CAS  PubMed Central  PubMed  Google Scholar 

  • Torres J, Rivera A, Clark G, Roux SJ (2008) Participation of extracellular nucleotides in the wound response of Dasycladus vermicularis and Acetabularia acetabulum (Dasycladales and Chlorophyta). J Phycol 44:1504–1511. doi:10.1111/j.1529-8817.2008.00602.x

    CAS  Google Scholar 

  • Tsitsigiannis DI, Keller NP (2007) Oxylipins as developmental host-fungal communication signals. Trends Microbiol 15(3):109–118. doi:10.1016/j.tim.2007.01.005

  • Watkins DN, Berman DM, Burkholder SG, Wang B, Beachy PA, Baylin SB (2003) Hedgehog signalling within airway epithelial progenitors in small-cell lung cancer. Nature 422:313–317. doi:10.1038/nature01493

    CAS  PubMed  Google Scholar 

  • White SR, Tse R, Marroquin BA (2005) Stress-activated protein kinases mediate cell migration in human airway epithelial cells. Am J Respir Cell Mol Biol 32:301–310. doi:10.1165/rcmb.2004-0118OC

    CAS  PubMed  Google Scholar 

  • Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24. doi:10.1146/annurev-genet-102209-163500

    CAS  PubMed  Google Scholar 

  • Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19(3):1096–1122. doi:10.1105/tpc.106.049353

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yoo SK, Huttenlocher A (2009) Innate Immunity: wounds burst H2O2 signals to leukocytes. Curr Biol 19(14):553–555. doi:10.1016/j.cub.2009.06.025

    Google Scholar 

  • Yuan P, Jedd G, Kumaran D, Swaminathan S, Shio H, Hewitt D, Chua AH, Swaminathan K (2003) A Hex-1 crystal lattice required for Woronin body function in Neurospora crassa. Nat Struct Biol 10(4):264–270. doi:10.1038/nsb910

    CAS  PubMed  Google Scholar 

  • Zeilinger S, Omann M (2007) Trichoderma biocontrol: signal transduction pathways involved in host sensing mycoparasitism. Gene Regul Syst Biol 1:227–234 (PMCID: PMC2759141)

  • Zeiser R, Penack O, Holler E, Idzko M (2011) Danger signals activating innate immunity in graft-versus-host disease. J Mol Med 89:833–845. doi:10.1007/s00109-011-0767-x

    CAS  PubMed  Google Scholar 

  • Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464(7285):104–107. doi:10.1038/nature08780

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao Z, Liu N, Huang J, Lu PH, Xu XM (2011) Inhibition of cPLA2 activation by Ginkgo biloba extract protects spinal cord neurons from glutamate excitotoxicity oxidative stress-induced cell death. J Neurochem 116:1057–1065. doi:10.1111/j.1471-4159.2010.07160.x

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zimmerman ZA, Kellogg DR (2001) The Sda1 protein is required for passage through start. Mol Biol Cell 12:201–219. doi:10.1091/mbc.12.1.201

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zorov DB, Bannikova SY, Belousov VV, Vyssokikh MY, Zorova LD, Isaev NK, Krasnikov BFY, Plotnikov E (2005) Reactive oxygen nitrogen species: friends or foes? Biochemistry (Mos) 70(2):215–221. doi:10.1007/s10541-005-0103-6

    CAS  Google Scholar 

Download references

Acknowledgments

Research related to the main subject of this review is supported by grant FOINS-CONACYT (I0110/193/10FON.INST. -30-10) to A H-E. This review article was supported in part by a grant from São Paulo Research Foundation (FAPESP) of Brazil # 2014/01229-4. The authors wish to thank Dr. Ana Calvo for allowing us to use an unpublished photograph obtained by her research group.

Author information

Authors and Affiliations

  1. Laboratorio Nacional de Genómica para la Biodiversidad, CINVESTAV-Irapuato, 36821, Irapuato, GTO, México

    M. A. Hernández-Oñate & A. Herrera-Estrella

Authors
  1. M. A. Hernández-Oñate
    View author publications

    Search author on:PubMed Google Scholar

  2. A. Herrera-Estrella
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to A. Herrera-Estrella.

Additional information

Communicated by D. E. N. Rangel.

This article is part of the Special Issue “Fungal Stress Responses”.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hernández-Oñate, M.A., Herrera-Estrella, A. Damage response involves mechanisms conserved across plants, animals and fungi. Curr Genet 61, 359–372 (2015). https://doi.org/10.1007/s00294-014-0467-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-014-0467-5

Keywords