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Mir1-CP, a novel defense cysteine protease accumulates in maize vascular tissues in response to herbivory

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Abstract

When lepidopteran larvae feed on the insect-resistant maize genotype Mp708 there is a rapid accumulation of a defensive cysteine protease, Maize insect resistance 1-cysteine protease (Mir1-CP), at the feeding site. Silver-enhanced immunolocalization visualized with both light and transmission electron microscopy was used to determine the location of Mir1-CP in the maize leaf. The results indicated that Mir1-CP is localized predominantly in the phloem of minor and intermediate veins. After 24 h of larval feeding, Mir1-CP increased in abundance in the vascular parenchyma cells and in the thick-walled sieve element (TSE); it was also found localized to the bundle sheath and mesophyll cells. In situ hybridization of mRNA encoding Mir1-CP indicated that the primary sites of Mir1-CP synthesis in the whorl are the vascular parenchyma and bundle sheath cells. In addition to the phloem, Mir1-CP was also found in the metaxylem of the leaf and root. After 24 h of foliar feeding, the amount of Mir1-CP in the root xylem increased and it appeared to move from xylem parenchyma into the root metaxylem elements. The accumulation of Mir1-CP in maize vascular elements suggests Mir1-CP may move through these tissues to defend against insect herbivores.

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Abbreviations

Mir1-CP:

Maize insect resistance 1-cysteine protease

FAW:

Fall armyworm

TSE:

Thick-walled sieve elements

References

  • Alvarez S, Goodger JQD, Marsh EL, Shen S, Asirvatham VS, Schatchman DP (2006) Characterization of the maize xylem sap proteome. J Proteome Res 5:963–972

    Article  PubMed  CAS  Google Scholar 

  • Barnes A, Bayle J, Constantinidou C, Ashton P, Jones A, Pritchard J (2004) Determinining protein identity from sieve element sap in Ricinus communis L. by quadrupole time of flight (Q-TOF) mass spectrometry. J Exp Bot 55:1473–1481

    Article  PubMed  CAS  Google Scholar 

  • Biles CL, Abeles FB (1991) Xylem sap proteins. Plant Physiol 96:597–601

    Article  PubMed  CAS  Google Scholar 

  • Beers BP, Woffenden BJ, Zhao C (2000) Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol Biol 44:399–415

    Article  PubMed  CAS  Google Scholar 

  • Chang Y-M, Luthe DS, Davis FM, Williams WP (1999) Influence of whorl region from resistant and susceptible corn genotypes on fall armyworm (Lepidoptera:Noctuide) growth and development. J Econ Entomol 93:477–483

    Article  Google Scholar 

  • Dannenhoffer JM, Suhr SC, Thompson GA (2001) Phloem-specific expression of the pumpkin fruit trypsin inhibitor. Planta 212:155–162

    Article  PubMed  CAS  Google Scholar 

  • Deom CM, Lapidot M, Beachy RN (1992) Plant virus movement proteins. Cell 69:221–224

    Article  PubMed  CAS  Google Scholar 

  • Evert RF, Eschrich W, Heyser W (1978) Leaf structure in relation to solute transport and phloem loading in Zea mays L. Planta 138:279–294

    Article  Google Scholar 

  • Funk V, Kositsup B, Zhao C, Beers EP (2002) The Arabidopsis xylem peptidase XCP1 is a tracheary element vacuolar protein that may be a papain ortholog. Plant Physiol 128:284

    Article  Google Scholar 

  • Goding JW (1980) Antibody production by hybridomas. J Immunol Methods 39:285–308

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto T, Yamada Y (1994) Alkaloid biogenesis: molecular aspects. Annu Rev Plant Physiol Plant Mol Biol 45:257–285

    CAS  Google Scholar 

  • Hause B, Hause G, Kutter C, Miersh O, Wasternack C (2003) Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant Cell Physiol 44:643–648

    Article  PubMed  CAS  Google Scholar 

  • Hooker JD (1874) The carnivorous habits of plants. Nature 10:366–372

    Google Scholar 

  • Kehr J (2006) Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J Exp Bot 57:767–774

    Article  PubMed  CAS  Google Scholar 

  • Knoblauch M, Peters WS, Ehlers K, van Bel AJE (2001) Reversible calcium-regulated stopcocks in legume sieve tubes. Plant Cell 13:1221–1230

    Article  PubMed  CAS  Google Scholar 

  • Konno K, Hirayama C, Nakamura M, Tateishi K, Tamura Y, Hattori M, Kohno K (2004) Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J 37:370–378

    Article  PubMed  CAS  Google Scholar 

  • Krüger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L, Jones JDG (2002) A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of tomato necrosis. Science 296:744–747

    Article  PubMed  Google Scholar 

  • la Cour Peterson ML, Hejgaard J, Thompson GA, Schulz A (2005) Cucurbit phloem serpins are graft-transmissible and appear to be resistant to turnover in the sieve element-companion cell complex. J Exp Bot 56:3111–3120

    Article  CAS  Google Scholar 

  • Lucas WJ, Gilbertson RL (1994) Plasmodesmata in relation to viral movement within leaf tissues. Annu Rev Phytopathol 32:387–411

    Article  CAS  Google Scholar 

  • Masuda S, Sakuta C, Satoh S (1999) cDNA cloning of a novel lectin-like xylem sap protein and its root-specific expression in cucumber. Plant Cell Physiol 40:1177–1181

    PubMed  CAS  Google Scholar 

  • Matsushima R, Hayashi Y, Kondo M, Shimada T, Nishimura M, Hara-Nishimura I (2002) An endoplasmic reticulum-derived structure that is induced under stress conditions in Arabidopsis. Plant Physiol 130:1807–1814

    Article  PubMed  CAS  Google Scholar 

  • Mohan S, Ma PKW, Pechan T, Bassford ER, Williams WP, Luthe DS (2005) Degradation of the Spodoptera frugiperda peritrophic matrix by an inducible maize cysteine protease. J Insect Physiol 52:21–28

    Article  PubMed  CAS  Google Scholar 

  • Murillo I, Cavallarin L, San-Segundo B (1997) The maize pathogenesis-related PRms protein localizes to plasmodesmata in maize radicles. Plant Cell 9:145–156

    Article  PubMed  CAS  Google Scholar 

  • Nakai K, Horton P (1999) PSORT: a program for detecting the sorting signals of proteins and predicting their subcellular localization. Trends Biochem Sci 24:34–35

    Article  PubMed  CAS  Google Scholar 

  • Narváez-Vásquez J, Pearce G, Ryan CA (2005) The plant cell wall matrix harbors a precursor of defense signaling peptides. Proc Natl Acad Sci (USA) 102:12974–12977

    Article  CAS  Google Scholar 

  • Ohira K, Ito T, Kawai A, Namba S, Kusumi T, Tsuchizaki T (1994) Nucleotide sequence of the 3′-terminal region of citrus tatter leaf virus RNA. Virus Genes 8:169–172

    Article  PubMed  CAS  Google Scholar 

  • Oparka KJ, Turgeon R (1999) Sieve elements and companion cells-traffic control centers of the phloem. Plant Cell 11:739–750

    Article  CAS  PubMed  Google Scholar 

  • Pechan T, Jiang BH, Steckler DS, Ye L, Lin L, Luthe DS, Williams WP (1999) Characterization of three distinct cDNA clones encoding cysteine proteinases from corn (Zea mays L.) callus. Plant Mol Biol 40:111–119

    Article  PubMed  CAS  Google Scholar 

  • Pechan T, Ye LJ, Chang YM, Mitra A, Lin L, Davis FM, Williams WP, Luthe DS (2000) A unique 33-kD cysteine proteinase accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other lepidoptera. Plant Cell 12:1031–1040

    Article  PubMed  CAS  Google Scholar 

  • Pechan T, Cohen A, Williams WP, Luthe DS (2002) Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. Proc Natl Acad Sci USA 99:13319–13323

    Article  PubMed  CAS  Google Scholar 

  • Pechan T, Ma PWK, Luthe DS (2004) Heterologous expression of maize (Zea mays L.) Mir-1 cysteine proteinase in eukaryotic and prokaryotic expression systems. Protein Expr Purif 34:134–141

    Article  PubMed  CAS  Google Scholar 

  • Plisson C, Drucker M, Blanc S, German-Retana S, Le Gall O, Thomas D, Bron P (2003) Structural characterization of HC-Pro, a plant virus multifunctional protein. J Biol Chem 278:23753–23761

    Article  PubMed  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  PubMed  CAS  Google Scholar 

  • Rojas MR, Zerbini FM, Allison RF, Gilbertson RL, Lucas WJ (1997) Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. Virology 237:293–295

    Article  Google Scholar 

  • Russell SH, Evert RF (1985) Leaf vasculature in Zea mays L. Planta 164:448–458

    Article  Google Scholar 

  • Ryan CA (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta 1477:112–121

    PubMed  CAS  Google Scholar 

  • Sakuta C, Satoh S (2000) Vascular tissue-specific gene expression of xylem sap glycine-rich proteins in root and their localization in the walls of metaxylem vessels cucumber. Plant Cell Physiol 41:627–638

    PubMed  CAS  Google Scholar 

  • Shoji T, Yamada Y, Hashimoto T (2000) Jasmonate induction of putrescine N-methyltransferase genes in the root of Nicotiana sylvestris. Plant Cell Physiol 41:831–839

    Article  PubMed  CAS  Google Scholar 

  • Singh AP, Srivastava LM (1971) The fine structure of corn phloem. Can J Bot 50:389–846

    Google Scholar 

  • Thompson GA, Schulz A (1999) Macromolecular trafficking in the phloem. Trends Plant Sci 4:354–360

    Article  PubMed  Google Scholar 

  • Turgeon R, Web JA, Evert RF (1975) Ultrastructure of minor veins in Cucurbita pepo leaves. Protoplasma 83:217–232

    Article  Google Scholar 

  • van Bel AJE, Ehlers K, Knoblauch M (2002) Sieve elements caught in the act. Trends Plant Sci 7:126–130

    Article  PubMed  Google Scholar 

  • van der Hoorn RAL, Jones JDG (2004) The plant proteolytic machinery and its role in defence. Curr Opin Plant Biol 7:400–407

    Article  PubMed  CAS  Google Scholar 

  • Walsh MA (1974) Late-formed metaphloem sieve-elements in Zea mays L. Planta 121:17–25

    Article  Google Scholar 

  • Walz C, Griavalisco P, Schad M, Juenge M, Klose J, Kehr J (2004) Proteomics of cucurbit phloem exudates reveals a network of defense proteins. Phytochemistry 65:1795–1804

    Article  PubMed  CAS  Google Scholar 

  • Williams WP, Davis FM, Windham GL (1990) Registration of Mp708 germplasm line of maize. Crop Sci 30:757

    Article  Google Scholar 

  • Yang T, Lev-Yadum S, Feldman M, Fromm H (1998) Developmentally regulated organ-, tissue-, and cell-specific expression of calmodulin genes in common wheat. Plant Mol Biol 37:109–120

    Article  PubMed  CAS  Google Scholar 

  • Yoshikawa N, Imaizumi M, Takahashi T, Inouye N (1993) Striking similarities between the nucleotide sequence and genome organization of citrus tatter leaf and apple stem grooving capilloviruses. J Gen Virol 74:2743–2747

    Article  PubMed  CAS  Google Scholar 

  • Zhang ZP, Baldwin IT (1997) Transport of [2-C-14] jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris. Planta 203:436–441

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Bill Monroe and Amanda Lawrence (Mississippi State University Electron Microscope Center) for their generous help and technical assistance. This research was supported by grant to DSL by the Life Sciences and Biotechnology Institute at Mississippi State University and the National Science Foundation (IBN-0236150). This is report J10807 of the Mississippi Agricultural and Forestry Experiment Station.

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Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, Mississippi State University, Box 9650, Mississippi State, MS, 39762, USA

    Lorena Lopez, Alberto Camas, Renuka Shivaji & Arunkanth Ankala

  2. Corn Host Plant Resistance Laboratory, USDA-ARS, Mississippi State University, Box 9555, Mississippi State, MS, 39762, USA

    Paul Williams

  3. Department of Crop and Soil Science, Pennsylvania State University, 116 ASI Building, University Park, PA, 16802, USA

    Dawn Luthe

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  1. Lorena Lopez
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  2. Alberto Camas
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  3. Renuka Shivaji
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  4. Arunkanth Ankala
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  5. Paul Williams
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  6. Dawn Luthe
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Correspondence to Dawn Luthe.

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Lorena Lopez and Alberto Camas contributed equally to the research and preparation of this manuscript.

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Lopez, L., Camas, A., Shivaji, R. et al. Mir1-CP, a novel defense cysteine protease accumulates in maize vascular tissues in response to herbivory. Planta 226, 517–527 (2007). https://doi.org/10.1007/s00425-007-0501-7

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  • DOI: https://doi.org/10.1007/s00425-007-0501-7

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