Calcium oxalate degradation is involved in aerenchyma formation in Typha angustifolia leaves
Xiaomin Du A , Xiaolong Ren A , Lingli Wang A B , Ke Yang A , Guiliang Xin A , Guolun Jia A , Xilu Ni C and Wenzhe Liu A DA Key Laboratory of Resource Biology and Biotechnology in Western China (Northwest University), Ministry of Education, School of Life Science, Northwest University, Xi’an 710069, China.
B Department of Life Sciences, Yuncheng University, Yuncheng 044000, China.
C State Key Laboratory of Seedling Bioengineering, Ningxia Forestry Institute, Yinchuan, 750004, China.
D Corresponding author. Email: lwenzhe@nwu.edu.cn
Functional Plant Biology 45(9) 922-934 https://doi.org/10.1071/FP17349
Submitted: 11 December 2017 Accepted: 5 March 2018 Published: 10 April 2018
Abstract
Typha angustifolia L. (Typhaceae) is an emergent aquatic plant, and aerenchyma is formed through cell lysis in its leaves. The developing aerenchyma of T. angustifolia contains many CaOx crystals (raphides). Oxalate oxidase (OXO) (oxalate : oxygen oxidoreductase, EC1.2.3.4) can degrades calcium oxalate to carbon dioxide and hydrogen peroxide (H2O2). High level of H2O2 acts as a key inducer for different types of developmentally and environmentally programmed cell death (PCD) and can promote the formation of aerenchyma. Therefore, the objective of this study was to describe the relationship between aerenchyma formation and the degradation of CaOx crystals. Light and transmission electron microscopy (TEM) results showed that CaOx crystals occurred between PCD-susceptible cells in the early phase of aerenchyma formation, and those cells and CaOx crystals were degraded at aerenchyma maturation. Cytochemical localisation was used to detect H2O2, and H2O2 was found in crystal idioblasts. In addition, the oxalate content, H2O2 content and OXO activity were determined. The results showed that the concentration of oxalate was the highest in the third cavity formation stage and the H2O2 concentration was also highest at this stage. Meanwhile, the activity of OXO was also high in the third cavity formation stage. TpOXO was highly expressed during the CaOx crystal degradation period by quantitative real-time PCR analysis. These results show that the degradation of CaOx crystals is involved in the regulation of the PCD process of aerenchyma. This study will contribute to understanding the changes in CaOx crystals during the formation of aerenchyma in T. angustifolia.
Additional keywords: calcium oxalate crystals, H2O2, oxalate oxidase, programmed cell death.
References
Ádám AL, Bestwick CS, Barna B, Mansfield JW (1995) Enzymes regulating the accumulation of active oxygen species during the hypersensitive reaction of bean to Pseudomonas syringae pv. phaseolicola. Planta 197, 240–249.| Enzymes regulating the accumulation of active oxygen species during the hypersensitive reaction of bean to Pseudomonas syringae pv. phaseolicola.Crossref | GoogleScholarGoogle Scholar |
Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773–784.
| Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXit1KlsLg%3D&md5=07b97418dc4ee2f6b02a050b43d5c873CAS |
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
| Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=187985f9d8c4a6274567637eb1db143eCAS |
Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Current Science 82, 1227–1238.
Bendix M, Tornbjerg T, Brix H (1994) Internal gas transport in Typha latifolia L. and Typha angustifolia L. 1. Humidity-induced pressurization and convective throughflow. Aquatic Botany 49, 75–89.
| Internal gas transport in Typha latifolia L. and Typha angustifolia L. 1. Humidity-induced pressurization and convective throughflow.Crossref | GoogleScholarGoogle Scholar |
Bestwick CS, Brown IR, Bennett MH, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. The Plant Cell 9, 209–221.
| Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhslGktb4%3D&md5=ff801c9779d84c7daf7916629b49289eCAS |
Caliskan M, Cuming AC (1998) Spatial specificity of H2O2-generating oxalate oxidase gene expression during wheat embryo germination. The Plant Journal 15, 165–171.
| Spatial specificity of H2O2-generating oxalate oxidase gene expression during wheat embryo germination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlslWqtrg%3D&md5=8822abbe3865157095ef85041df0fbebCAS |
Chamnongpol S, Willekens H, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1996) Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. The Plant Journal 10, 491–503.
| Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtF2lt7w%3D&md5=187293ce4ff7c4242e88d2bdbf987d50CAS |
Coté GG (2009) Diversity and distribution of idioblasts producing calcium oxalate crystals in Dieffenbachia seguine (Araceae). American Journal of Botany 96, 1245–1254.
| Diversity and distribution of idioblasts producing calcium oxalate crystals in Dieffenbachia seguine (Araceae).Crossref | GoogleScholarGoogle Scholar |
De Pinto MC, Locato V, De Gara L (2012) Redox regulation in plant programmed cell death. Plant, Cell & Environment 35, 234–244.
| Redox regulation in plant programmed cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtVKns7c%3D&md5=5f910df5a858ed0db4601544dae6cc33CAS |
de Oliveira Ceita GO, Macêdo JNA, Santos TB, Alemanno L, da Silva Gesteira A, Micheli F, Mariano AC, Gramacho KP, Silva DC, Meinhardt L, Mazzafera P, Pereira GAG, Cascardo JCM (2007) Involvement of calcium oxalate degradation during programmed cell death in Theobroma cacao tissues triggered by the hemibiotrophic fungus Moniliophthora perniciosa. Plant Science 173, 106–117.
| Involvement of calcium oxalate degradation during programmed cell death in Theobroma cacao tissues triggered by the hemibiotrophic fungus Moniliophthora perniciosa.Crossref | GoogleScholarGoogle Scholar |
Franceschi V (2001) Calcium oxalate in plants. Trends in Plant Science 6, 331
| Calcium oxalate in plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MznvFGrsA%3D%3D&md5=c60166ab653262c7612785c054c83d1bCAS |
Franceschi VR, Horner HT (1980) Calcium oxalate crystals in plants. Botanical Review 46, 361–427.
| Calcium oxalate crystals in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtFKitg%3D%3D&md5=d893400a65e7196704985644f908017aCAS |
Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Annual Review of Plant Biology 56, 41–71.
| Calcium oxalate in plants: formation and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVaru74%3D&md5=05c4efe71986d7be9485781e7104aefcCAS |
Gallaher RN (1975) The occurrence of calcium in plant tissue as crystals of calcium oxalate. Communications in Soil Science and Plant Analysis 6, 315–330.
| The occurrence of calcium in plant tissue as crystals of calcium oxalate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXlt1ylsL8%3D&md5=79b6a3e698fd3012dd9d20954673a226CAS |
Gechev TS, Hille J (2005) Hydrogen peroxide as a signal controlling plant programmed cell death. Journal of Cell Biology 168, 17–20.
| Hydrogen peroxide as a signal controlling plant programmed cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltlSqsA%3D%3D&md5=1a41526294f3b881f6306fe40e3ba751CAS |
Gechev TS, Gadjev IZ, Hille J (2004) An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants. Cellular and Molecular Life Sciences 61, 1185–1197.
| An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXls1aqsLo%3D&md5=7382245d05146c6bfb368a442cf234c5CAS |
Gechev T, Minkov I, Hille J (2005) Hydrogen peroxide-induced cell death in Arabidopsis: transcriptional and mutant analysis reveals a role of an oxoglutarate-dependent dioxygenase gene in the cell death process. IUBMB Life 57, 181–188.
| Hydrogen peroxide-induced cell death in Arabidopsis: transcriptional and mutant analysis reveals a role of an oxoglutarate-dependent dioxygenase gene in the cell death process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvFaisb8%3D&md5=d59e38d9f8119b2e36047e7a895cc118CAS |
Gui MY, Liu WZ (2014) Programmed cell death during floral nectary senescence in Ipomoea purpurea. Protoplasma 251, 677–685.
| Programmed cell death during floral nectary senescence in Ipomoea purpurea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmvFCmtbw%3D&md5=ccaf3c14afab2ee1b65817219f8a8a5cCAS |
Havir EA, Anagnostakis SL (1983) Oxalate production by virulent but not by hypovirulent strains of Endothia parasitica. Physiological Plant Pathology 23, 369–376.
| Oxalate production by virulent but not by hypovirulent strains of Endothia parasitica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmsVOjuw%3D%3D&md5=4e6875e70d9d4d6b3fd33ae9f66f5d69CAS |
Horner HT, Wagner BL (1980) The association of druse crystals with the developing stomium of Capsicum annuum (Solanaceae) anthers. American Journal of Botany 67, 1347–1360.
| The association of druse crystals with the developing stomium of Capsicum annuum (Solanaceae) anthers.Crossref | GoogleScholarGoogle Scholar |
Horner HT, Wagner BL (1995) Calcium oxalate formation in higher plants. Calcium Oxalate in Biological Systems 1, 53–72.
Horner HT, Wanke S, Samain MS (2012) A comparison of leaf crystal macropatterns in the two sister genera Piper and Peperomia (Piperaceae). American Journal of Botany 99, 983–997.
| A comparison of leaf crystal macropatterns in the two sister genera Piper and Peperomia (Piperaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFGjtrrL&md5=495d5189037bda4707c7769e68ae18d5CAS |
Hu X, Bidney DL, Yalpani N, Duvick JP, Crasta O, Folkerts O, Lu G (2003) Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiology 133, 170–181.
| Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlaitLc%3D&md5=375cede0271f630a5c04f77b8bd93a57CAS |
Hung KT, Kao CH (2007) The participation of hydrogen peroxide in methyl jasmonate-induced NH4 + accumulation in rice leaves. Journal of Plant Physiology 164, 1469–1479.
| The participation of hydrogen peroxide in methyl jasmonate-induced NH4 + accumulation in rice leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlKktL7N&md5=5b8650189bf5a566f904b678b3731dfdCAS |
Jin ZX, Wang CH, Chen WF, Chen XY, Li XZ (2007) Induction of oxalate decarboxylase by oxalate in a newly isolated Pandoraea sp. OXJ-11 and its ability to protect against Sclerotinia sclerotiorum infection. Canadian Journal of Microbiology 53, 1316–1322.
| Induction of oxalate decarboxylase by oxalate in a newly isolated Pandoraea sp. OXJ-11 and its ability to protect against Sclerotinia sclerotiorum infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVensLc%3D&md5=dcb2d15eaf45128954416a9e78539c52CAS |
Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annual Review of Plant Biology 48, 251–275.
| The oxidative burst in plant disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1entr8%3D&md5=7b961f0b0f2fead6320ecfcbefe3250bCAS |
Lane BG (1994) Oxalate, germin, and the extracellular matrix of higher plants. FASEB Journal 8, 294–301.
| Oxalate, germin, and the extracellular matrix of higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXis1GksLY%3D&md5=cd7d69e907d185aa8241b812d5c51d04CAS |
Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC (1993) Germin, a protein marker of early plant development, is an oxalate oxidase. The Journal of Biological Chemistry 268, 12239–12242.
Le Deunff E, Davoine C, Le Dantec C, Billard JP, Huault C (2004) Oxidative burst and expression of germin/oxo genes during wounding of ryegrass leaf blades: comparison with senescence of leaf sheaths. The Plant Journal 38, 421–431.
| Oxidative burst and expression of germin/oxo genes during wounding of ryegrass leaf blades: comparison with senescence of leaf sheaths.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksleqtLw%3D&md5=720f93f747b00f40eb2f44d36fc03a71CAS |
Libert B, Franceschi VR (1987) Oxalate in crop plants. Journal of Agricultural and Food Chemistry 35, 926–938.
| Oxalate in crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXmtFCktb0%3D&md5=95f3480a5348e82258f6366fd24e3f9eCAS |
Liu F, Wang M, Wen J, Yi B, Shen J, Ma C, Tu J, Fu T (2015) Overexpression of barley oxalate oxidase gene induces partial leaf resistance to Sclerotinia sclerotiorum in transgenic oilseed rape. Plant Pathology 64, 1407–1416.
| Overexpression of barley oxalate oxidase gene induces partial leaf resistance to Sclerotinia sclerotiorum in transgenic oilseed rape.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVOnu73P&md5=cff715b15414e3d93d70de62de0437edCAS |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔC T method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔC T method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=66c09ccfc1a1f4063babd93cb6f93672CAS |
Mayo SJ (1989) Observations of gynoecial structure in Philodendron (Araceae). Botanical Journal of the Linnean Society 100, 139–172.
| Observations of gynoecial structure in Philodendron (Araceae).Crossref | GoogleScholarGoogle Scholar |
Mazen AMA, Zhang D, Franceschi VR (2004) Calcium oxalate formation in Lemna minor: physiological and ultrastructural aspects of high capacity calcium sequestration. New Phytologist 161, 435–448.
| Calcium oxalate formation in Lemna minor: physiological and ultrastructural aspects of high capacity calcium sequestration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVymurc%3D&md5=77b604fb82ce75fbe13d3a6435069174CAS |
McNair JB (1932) The interrelation between substances in plants: essential oils and resins, cyanogen and oxalate. American Journal of Botany 19, 255–272.
| The interrelation between substances in plants: essential oils and resins, cyanogen and oxalate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaA38Xjs1Krtw%3D%3D&md5=b622f7756f5359629d27eb90821ad990CAS |
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880.
Ni XL, Meng Y, Zheng SS, Liu WZ (2014) Programmed cell death during aerenchyma formation in Typha angustifolia leaves. Aquatic Botany 113, 8–18.
| Programmed cell death during aerenchyma formation in Typha angustifolia leaves.Crossref | GoogleScholarGoogle Scholar |
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59, 368–373.
| Polychromatic staining of plant cell walls by toluidine blue O.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2MXmtVOmsw%3D%3D&md5=d9ee75f07bf9266be82183b8ac52d50bCAS |
Paranidharan V, Palaniswami A, Vidhyasekaran P, Velazhahan R (2003) Induction of enzymatic scavengers of active oxygen species in rice in response to infection by Rhizoctonia solani. Acta Physiologiae Plantarum 25, 91–96.
| Induction of enzymatic scavengers of active oxygen species in rice in response to infection by Rhizoctonia solani.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvFGlsro%3D&md5=e1d3779000301ddccd3f9494bcfff503CAS |
Prychid CJ, Rudall PJ (1999) Calcium oxalate crystals in monocotyledons: a review of their structure and systematics. Annals of Botany 84, 725–739.
| Calcium oxalate crystals in monocotyledons: a review of their structure and systematics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotVGitbs%3D&md5=0a735a2c9f8b659ccec37fd925708b75CAS |
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany 53, 1305–1319.
| Regulation and function of ascorbate peroxidase isoenzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFSls7Y%3D&md5=27e0366459fe787ac68c44d91b864930CAS |
Steffens B, Geske T, Sauter M (2011) Aerenchyma formation in the rice stem and its promotion by H2O2. New Phytologist 190, 369–378.
| Aerenchyma formation in the rice stem and its promotion by H2O2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmt1Gktb4%3D&md5=184893100dbde4079f12201b93b91064CAS |
Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Current Opinion in Plant Biology 14, 691–699.
| Respiratory burst oxidases: the engines of ROS signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFygu7vJ&md5=c606f2f6d6a9ad1eaf4ad32c883c0733CAS |
Teakle NL, Armstrong J, Barrett-Lennard EG, Colmer TD (2011) Aerenchymatous phellem in hypocotyl and roots enables O2 transport in Melilotus siculus. New Phytologist 190, 340–350.
| Aerenchymatous phellem in hypocotyl and roots enables O2 transport in Melilotus siculus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmt1GktLY%3D&md5=dac157bfe4890d65963cc1bbaabd3a49CAS |
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. The Plant Journal 11, 1187–1194.
| Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkslajtLs%3D&md5=40c3e5df0584c58bf0e3dae220c59377CAS |
Tornberg T, Bendix M, Brix H (1994) Internal gas transport in Typha latifolia L. and Typha angustifolia L. 2. Convective throughflow pathways and ecological significance. Aquatic Botany 49, 91–105.
| Internal gas transport in Typha latifolia L. and Typha angustifolia L. 2. Convective throughflow pathways and ecological significance.Crossref | GoogleScholarGoogle Scholar |
Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M, Inzé D, Van Breusegem F (2004) Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. The Plant Journal 39, 45–58.
| Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1ykur4%3D&md5=38334621287a609a311ec8ab8974d14fCAS |
Volk GM, Lynch-Holm VJ, Kostman TA, Goss LJ, Franceschi VR (2002) The role of druse and raphide calcium oxalate crystals in tissue calcium regulation in Pistia stratiotes leaves. Plant Biology 4, 34–45.
| The role of druse and raphide calcium oxalate crystals in tissue calcium regulation in Pistia stratiotes leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisFGltr4%3D&md5=a7b0b491ea8f62f87f16e5fce38fcdb0CAS |
Wakabayashi K, Soga K, Hoson T (2011) Cell wall oxalate oxidase modifies the ferulate metabolism in cell walls of wheat shoots. Journal of Plant Physiology 168, 1997–2000.
| Cell wall oxalate oxidase modifies the ferulate metabolism in cell walls of wheat shoots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFyns7jF&md5=00f27a79914cd6dfe63ee692e60b1ff5CAS |
Wang J, Zhang H, Allen RD (1999) Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant & Cell Physiology 40, 725–732.
| Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkvVaqu70%3D&md5=938663e919942d511f1641aaabd725f1CAS |
Xu QT, Yang L, Zhou ZQ, Mei FZ, Qu LH, Zhou GS (2013) Process of aerenchyma formation and reactive oxygen species induced by waterlogging in wheat seminal roots. Planta 238, 969–982.
| Process of aerenchyma formation and reactive oxygen species induced by waterlogging in wheat seminal roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtleku7%2FO&md5=caa4111288db123ba9b29843c8f4376eCAS |
Yamauchi T, Rajhi I, Nakazono M (2011) Lysigenous aerenchyma formation in maize root is confined to cortical cells by regulation of genes related to generation and scavenging of reactive oxygen species. Plant Signaling & Behavior 6, 759–761.
| Lysigenous aerenchyma formation in maize root is confined to cortical cells by regulation of genes related to generation and scavenging of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitlOhsLs%3D&md5=05b1989067be713b1b895ac91d13a0c2CAS |
Yao N, Tada Y, Park P, Nakayashiki H, Tosa Y, Mayama S (2001) Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats. The Plant Journal 28, 13–26.
| Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosVWqsrg%3D&md5=5bc93c20e29a2713176e0454100ca2f2CAS |
Zhang LH, Li PJ, Li XM, Meng XL, Xu CB (2005) Effects of cadmium stress on the growth and physiological characteristics of wheat seedlings. Shengtaixue Zazhi 24, 458–460.