The involvement of programmed cell death in inflated leaf petiole morphogenesis in Trapa pseudoincisa
Xi-Lu Ni A B C , Ling-ling Tan D , Ya-fu Zhou E , Wen-zhe Liu B F and Chang-xiao Li A F
+ Author Affiliations
- Author Affiliations
A Key Laboratory for the Eco-Environment of the Three Gorges Reservoir Region of the Ministry of Education, College of Life Sciences, Southwest University, Chongqing 400715, China.
B School of Life Science, Northwest University, Xi’an 710069, China.
C State Key Laboratory of Seedling Bioengineering, Ningxia Forestry Institute, Yinchuan 750004, China.
D College of Life Science, Qingdao Agricultural University, Qingdao 266109, China.
E Xi’an Botanical Garden of Shaanxi Province, Institute of Botany of Shaanxi Province, Xi’an 710061, China.
F Corresponding authors. Email: lwenzhe@nwu.edu.cn; lichangx@swu.edu.cn
Functional Plant Biology 45(4) 412-427 https://doi.org/10.1071/FP17203
Submitted: 20 July 2017 Accepted: 10 October 2017 Published: 20 November 2017
Abstract
Trapa plants (Trapaceae) have an inflated leaf petiole called a spongy airbag. The aims of this study were to assess the involvement of programmed cell death (PCD) in the process of inflated leaf petiole morphogenesis. In this paper, light and transmission electron microscopy (TEM) were used to investigate cytological events and the development of inflated leaf petiole. During this process, the inflated leaf petiole of Trapa pseudoincisa L. undergoes a developmental process, changing from solid to hollow phase. Debris from the degraded cells was seldom observed in the transverse sections of leaf petioles, but some degraded cells with an abnormal morphology were observed in longitudinal sections. Cytoplasmic changes, such as disrupted vacuoles, degraded plastids, and the emergence of secondary vacuoles were observed during leaf petiole morphogenesis. In addition, gel electrophoresis and TUNEL assays were used to evaluate DNA cleavage during petiole morphogenesis. DNA internucleosomal cleavage and TUNEL-positive nuclei indicate that the typical PCD features of DNA cleavage occurred early in the process. These results revealed that PCD plays a critical role in inflated leaf petiole morphogenesis. Additionally, a trans-disciplinary systems approach is required that recognises the necessity for integration of cytological and molecular characteristics for identification of aerenchyma type.
Additional keywords: inflated leaf petiole morphogenesis, lysigenous aerenchyma, PCD.
References
Armstrong W (1979) Aeration in higher plants. Advances in Botanical Research 7, 225–332.| Aeration in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhsVeiu7c%3D&md5=bd7ac671ff6c7a11056c42b86a2c3f67CAS |
Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313–339.
| Flooding stress: acclimations and genetic diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsLc%3D&md5=d90a6c2ec0e60f70cf1ac88123e7f803CAS |
Bartoli G, Forino LMC, Durante M, Tagliasacchi AM (2015) A lysigenic programmed cell death-dependent process shapes schizogenously formed aerenchyma in the stems of the waterweed Egeria densa. Annals of Botany 116, 91–99.
| A lysigenic programmed cell death-dependent process shapes schizogenously formed aerenchyma in the stems of the waterweed Egeria densa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MfmsF2nuw%3D%3D&md5=c8e7f4d475494d62ca35cfc990238facCAS |
Cao J, He XE, Wang YQ, Cui KM (2003) Programmed cell death during secondary xylem differentiation in Eucommia ulmoides. Journal of Integrative Plant Biology 45, 1465–1474.
Cardoso JA, Rincón J, Jiménez JDLC, Noguera D, Rao IM (2013) Morpho-anatomical adaptations to waterlogging by germplasm accessions in a tropical forage grass. AoB Plants 5, plt047
| Morpho-anatomical adaptations to waterlogging by germplasm accessions in a tropical forage grass.Crossref | GoogleScholarGoogle Scholar |
Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36, 665–681.
| Flooding tolerance: suites of plant traits in variable environments.Crossref | GoogleScholarGoogle Scholar |
Dauphinee A, Wright H, Rantong G, Gunawardena A (2012) The involvement of ethylene in programmed cell death and climacteric-like behaviour during the remodelling of lace plant (Aponogeton madagascariensis) leaves. Botany 90, 1237–1244.
| The involvement of ethylene in programmed cell death and climacteric-like behaviour during the remodelling of lace plant (Aponogeton madagascariensis) leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1ajsb3M&md5=9f7e72e7eef7367c67bcadc286b13886CAS |
Dauphinee AN, Warner TS, Gunawardena AH (2014) A comparison of induced and developmental cell death morphologies in lace plant (Aponogeton madagascariensis) leaves. BMC Plant Biology 14, 389
| A comparison of induced and developmental cell death morphologies in lace plant (Aponogeton madagascariensis) leaves.Crossref | GoogleScholarGoogle Scholar |
Domínguez F, Moreno J, Cejudo FJ (2012) The scutellum of germinated wheat grains undergoes programmed cell death: identification of an acidic nuclease involved in nucleus dismantling. Journal of Experimental Botany 63, 5475–5485.
| The scutellum of germinated wheat grains undergoes programmed cell death: identification of an acidic nuclease involved in nucleus dismantling.Crossref | GoogleScholarGoogle Scholar |
Drew MC, He CJ, Morgan PW (2000) Programmed cell death and aerenchyma formation in roots. Trends in Plant Science 5, 123–127.
| Programmed cell death and aerenchyma formation in roots.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvnslKntw%3D%3D&md5=09a6b99eef86ae3b740f1ece7befab5cCAS |
Evans DE (2004) Tansley review. Aerenchyma formation. New Phytologist 161, 35–49.
| Tansley review. Aerenchyma formation.Crossref | GoogleScholarGoogle Scholar |
Filonova LH, Bozhkov PV, Brukhin VB, Daniel G, Zhivotovsky B, Von AS (2000) Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce. Journal of Cell Science 113, 4399–4411.
Fukuda H (2000) Programmed cell death of tracheary elements as a paradigm in plants. Plant Molecular Biology 44, 245–253.
| Programmed cell death of tracheary elements as a paradigm in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtFWqtA%3D%3D&md5=674ec1b1c302ba6eed77605dd6b32023CAS |
Gray J (2004) ‘Programmed cell death in plants.’ (Blackwell Publishing: Oxford)
Groover A, Jones AM (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiology 119, 375–384.
| Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFSlurs%3D&md5=d015d6e550fb5e01655358b6ef7e5802CAS |
Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001a) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212, 205–214.
| Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1Kkuw%3D%3D&md5=5f768ecc24a2f078678a335d78330e49CAS |
Gunawardena A, Jackson M, Hawes C, Evans D (2001b) Rapid changes in cell wall pectic polysaccharides are closely associated with early stages of aerenchyma formation, a spatially localized form of programmed cell death in roots of maize (Zea mays L.) promoted by ethylene. Plant, Cell & Environment 24, 1369–1375.
| Rapid changes in cell wall pectic polysaccharides are closely associated with early stages of aerenchyma formation, a spatially localized form of programmed cell death in roots of maize (Zea mays L.) promoted by ethylene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisFCluw%3D%3D&md5=e467cff6729c039f2fe7b276cd9a6214CAS |
Gunawardena AH, Greenwood JS, Dengler NG (2004) Programmed cell death remodels lace plant leaf shape during development. The Plant Cell 16, 60–73.
| Programmed cell death remodels lace plant leaf shape during development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXosVemuw%3D%3D&md5=053adf097aa7e9733ba5c56ee93bfd8aCAS |
Gunawardena AH, Sault K, Donnelly P, Greenwood JS, Dengler NG (2005) Programmed cell death and leaf morphogenesis in Monstera obliqua (Araceae). Planta 221, 607–618.
| Programmed cell death and leaf morphogenesis in Monstera obliqua (Araceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVymsbo%3D&md5=5bfee5d853e2360b3839d9c870e5b28bCAS |
He C, Finlayson SA, Drew MC, Jordan WR, Morgan PW (1996) Ethylene biosynthesis during aerenchyma formation in roots of maize subjected to mechanical impedance and hypoxia. Plant Physiology 112, 1679–1685.
| Ethylene biosynthesis during aerenchyma formation in roots of maize subjected to mechanical impedance and hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlsVSj&md5=574d6c377e7dca15cd4c77fc10e3ac2bCAS |
Hu Z, Qi X, Zhang M, Chen X, Nakazono M (2016) Roles of phytohormones in morphological and anatomical responses of plants to flooding stress. In ‘Plant hormones under challenging environmental factors’. (Eds G Ahammed, JQ Yu) pp. 117–132. (Springer: Dordrecht, The Netherlands)
Jackson MB, Drew MC (1984) Effects of flooding on growth and metabolism of herbaceous plants. In ‘Flooding and plant growth’. (Ed. TT Kozlowsky) pp. 47–128. (Academic Press: Orlando)
Jones AM (2001) Programmed cell death in development and defense. Plant Physiology 125, 94–97.
| Programmed cell death in development and defense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslymtLc%3D&md5=f7ef29a70e284ced45c80410af318a29CAS |
Jung J, Lee SC, Choi HK (2008) Anatomical patterns of aerenchyma in aquatic and wetland plants. Journal of Plant Biology 51, 428–439.
| Anatomical patterns of aerenchyma in aquatic and wetland plants.Crossref | GoogleScholarGoogle Scholar |
Justin SHFW, Armstrong W (1991) Evidence for the involvement of ethene in aerenchyma formation in adventitious roots of rice (Oryza sativa L.). New Phytologist 118, 49–62.
| Evidence for the involvement of ethene in aerenchyma formation in adventitious roots of rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFGit7g%3D&md5=9cca083006d67d8f13dbbf70d9e035a3CAS |
Kong Y, Wang Z, Chen J, Pan XT, Liu DT, Zhang EJ (2009) Effects of ethephon on aerenchyma formation in rice roots. Rice Science 16, 210–216.
| Effects of ethephon on aerenchyma formation in rice roots.Crossref | GoogleScholarGoogle Scholar |
Laan P, Berrevoets MJ, Lythe S, Armstrong W, Cwpm B (1989) Root morphology and aerenchyma formation as indicators of the flood-tolerance of Rumex species. Journal of Ecology 77, 693–703.
| Root morphology and aerenchyma formation as indicators of the flood-tolerance of Rumex species.Crossref | GoogleScholarGoogle Scholar |
Liang F, Shen LZ, Chen M, Yang Q (2008) Formation of intercellular gas space in the diaphragm during the development of aerenchyma in the leaf petiole of Sagittaria trifolia. Aquatic Botany 88, 185–195.
| Formation of intercellular gas space in the diaphragm during the development of aerenchyma in the leaf petiole of Sagittaria trifolia.Crossref | GoogleScholarGoogle Scholar |
Liu Y, Schiff M, Czymmek K, Tallóczy Z, Levine B, Dinesh-Kumar SP (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121, 567–577.
| Autophagy regulates programmed cell death during the plant innate immune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkslelsLw%3D&md5=56eda71ebec929e0f564331f969b7325CAS |
Liu WZ, Zhou YF, Wang X, Jiao ZJ (2010) Programmed cell death during pigment gland formation in Gossypium hirsutum leaves. Plant Biology 12, 895–902.
| Programmed cell death during pigment gland formation in Gossypium hirsutum leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVantrjK&md5=6094fd461a36881664679eefa8b40815CAS |
López-Fernández MP, Maldonado S (2013) Programmed cell death during quinoa perisperm development. Journal of Experimental Botany 64, 3313–3325.
| Programmed cell death during quinoa perisperm development.Crossref | GoogleScholarGoogle Scholar |
Mahlberg PG (1972) Further observations on the phenomenon of secondary vacuolation in living cells. American Journal of Botany 59, 172–179.
| Further observations on the phenomenon of secondary vacuolation in living cells.Crossref | GoogleScholarGoogle Scholar |
Mahlberg PG, Olson K, Walkinshaw C (1970) Development of peripheral vacuoles in plant cells. American Journal of Botany 57, 962–968.
| Development of peripheral vacuoles in plant cells.Crossref | GoogleScholarGoogle Scholar |
Mahlberg PG, Olson K, Walkinshaw C (1971) Origin and development of plasma membrane derived invaginations in Vinca rosea L. American Journal of Botany 58, 407–416.
| Origin and development of plasma membrane derived invaginations in Vinca rosea L.Crossref | GoogleScholarGoogle Scholar |
Mahlberg PG, Turner F, Walkinshaw C, Venketeswaran S (1974) Ultrastructural studies plasma membrane related secondary vacuoles in cultured cells. American Journal of Botany 61, 730–738.
| Ultrastructural studies plasma membrane related secondary vacuoles in cultured cells.Crossref | GoogleScholarGoogle Scholar |
Nakashima J, Takabe K, Fujita M, Fukuda H (2000) Autolysis during in vitro tracheary element differentiation: formation and location of the perforation. Plant & Cell Physiology 41, 1267–1271.
| Autolysis during in vitro tracheary element differentiation: formation and location of the perforation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVKgu74%3D&md5=966f37297566b4034748efed0f642c25CAS |
Nedukha OM, Kotenko TB (2012) Heterophylly of Trapa natans L. Morphological and anatomical structure of leaves. Modern Phytomorphology 2, 29–33.
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 |
Ni XL, Shu H, Zhou YF, Wang FH, Liu WZ (2015) Leaf-shape remodeling: programmed cell death in fistular leaves of Allium fistulosum. Physiologia Plantarum 153, 419–431.
| Leaf-shape remodeling: programmed cell death in fistular leaves of Allium fistulosum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXivFSqs7o%3D&md5=a0d4252507952ed1f03eb7cdc56e43bcCAS |
Purnobasuki H, Suzuki M (2005) Aerenchyma tissue development and gas-pathway structure in root of Avicennia marina (Forsk.) Vierh. Journal of Plant Research 118, 285–294.
| Aerenchyma tissue development and gas-pathway structure in root of Avicennia marina (Forsk.) Vierh.Crossref | GoogleScholarGoogle Scholar |
Reape TJ, McCabe PF (2008) Apoptotic-like programmed cell death in plants. New Phytologist 180, 13–26.
| Apoptotic-like programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ait7nI&md5=c6eb4a755ef7325ecf99a475e2fbcfc4CAS |
Reape TJ, Molony EM, Mccabe PF (2008) Programmed cell death in plants: distinguishing between different modes. Journal of Experimental Botany 59, 435–444.
| Programmed cell death in plants: distinguishing between different modes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVamu7g%3D&md5=beefa39a2fec459cd08051115699c1abCAS |
Roberts K, Mccann MC (2000) Xylogenesis: the birth of a corpse. Current Opinion in Plant Biology 3, 517–522.
| Xylogenesis: the birth of a corpse.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FmtFejsQ%3D%3D&md5=c0e6389193f01bbf625557250ecedcbbCAS |
Sarkar P, Gladish DK (2012) Hypoxic stress triggers a programmed cell death pathway to induce vascular cavity formation in Pisum sativum roots. Physiologia Plantarum 146, 413–426.
| Hypoxic stress triggers a programmed cell death pathway to induce vascular cavity formation in Pisum sativum roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKlurrI&md5=fedb373ac620e2cc7f8d7760c1df65bcCAS |
Schussler EE, Longstreth DJ (1996) Aerenchyma develops by cell lysis in roots and cell separation in leaf petioles in Sagittaria lancifolia (Alismataceae). American Journal of Botany 83, 1266–1273.
| Aerenchyma develops by cell lysis in roots and cell separation in leaf petioles in Sagittaria lancifolia (Alismataceae).Crossref | GoogleScholarGoogle Scholar |
Seago JL, Peterson CA, Enstone DE, Scholey CA (1999) Development of the endodermis and hypodermis of Typha glauca Godr. and Typha angustifolia L. roots. Canadian Journal of Botany 77, 122–134.
| Development of the endodermis and hypodermis of Typha glauca Godr. and Typha angustifolia L. roots.Crossref | GoogleScholarGoogle Scholar |
Seago JJ, Peterson CA, Enstone DE (2000) Cortical development in roots of the aquatic plant Pontederia cordata (Pontederiaceae). American Journal of Botany 87, 1116–1127.
| Cortical development in roots of the aquatic plant Pontederia cordata (Pontederiaceae).Crossref | GoogleScholarGoogle Scholar |
Seago J, Marsh L, Stevens K, Soukup A, Votrubova O, Enstone D (2005) A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma. Annals of Botany 96, 565–579.
| A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma.Crossref | GoogleScholarGoogle Scholar |
Shiono K, Ogawa S, Yamazaki S, Isoda H, Fujimura T, Nakazono M, Colmer TD (2011) Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths. Annals of Botany 107, 89–99.
| Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2rsrrO&md5=f60f1af107d10976d52a76db8958b539CAS |
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=c02d846fb3570ebfb818f403c81ed9a5CAS |
Takahashi H, Yamauchi T, Colmer TD, Nakazono M (2014) Aerenchyma formation in plants. In ‘Low-oxygen stress in plants’. (Eds JT Dongen, F Licausi) pp. 247–265. (Springer-Verlag: Wien, Germany)
Thomas A, Guerreiro S, Sodek L (2005) Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean. Annals of Botany 96, 1191–1198.
| Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MnhsVCgsg%3D%3D&md5=db83d9a6841fa206a75aecec8ec2a2b4CAS |
Trought MCT, Drew MC (1980) The development of waterlogging damage in young wheat plants in anaerobic solution cultures. Journal of Experimental Botany 31, 1573–1585.
| The development of waterlogging damage in young wheat plants in anaerobic solution cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhtlKgt7o%3D&md5=6ce8dd65ceef79c57c07248ae32f7776CAS |
Voesenek LACJ, Rijnders JHGM, Peeters AJM, van de Steeg HM, De Kroon H (2004) Plant hormones regulate fast shoot elongation under water: from genes to communities. Ecology 85, 16–27.
| Plant hormones regulate fast shoot elongation under water: from genes to communities.Crossref | GoogleScholarGoogle Scholar |
Wertman J, Lord CCEN, Dauphinee AN, Gunawardena AH (2012) The pathway of cell dismantling during programmed cell death in lace plant (Aponogeton madagascariensis) leaves. BMC Plant Biology 12, 115
| The pathway of cell dismantling during programmed cell death in lace plant (Aponogeton madagascariensis) leaves.Crossref | GoogleScholarGoogle Scholar |
Yamamoto R, Demura T, Fukuda H (1997) Brassinosteroids induce entry into the final stage of tracheary element differentiation in cultured Zinnia cells. Plant & Cell Physiology 38, 980–983.
| Brassinosteroids induce entry into the final stage of tracheary element differentiation in cultured Zinnia cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlsVGnsr8%3D&md5=faf7a34f7e9a7f625b1dc450fe7aa52dCAS |
Yamauchi T, Watanabe K, Fukazawa A, Mori H, Abe F, Kawaguchi K, Oyanagi A, Nakazono M (2014) Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions. Journal of Experimental Botany 65, 261–273.
| Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlvF2jtw%3D%3D&md5=6cb7136ebbf17832302e235a2d0a6452CAS |
Yan SZ, Leng JF, Liu ZQ (1993) A study on the ecological anatomy of stem of Trapa acornis nakai at water levels of different depth. Journal of Nanjing Normal University 16, 50–54.
Yin D, Chen S, Chen F, Jiang J (2013) Ethylene promotes induction of aerenchyma formation and ethanolic fermentation in waterlogged roots of Dendranthema spp. Molecular Biology Reports 40, 4581–4590.
| Ethylene promotes induction of aerenchyma formation and ethanolic fermentation in waterlogged roots of Dendranthema spp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXps1Cmtrg%3D&md5=b18acf73bf331aabb27616ff7ed214deCAS |
Young TE, Gallie DR (1999) Analysis of programmed cell death in wheat endosperm reveals differences in endosperm development between cereals. Plant Molecular Biology 39, 915–926.
| Analysis of programmed cell death in wheat endosperm reveals differences in endosperm development between cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjt1Sqt7s%3D&md5=cff601d6c7e6d5578f241a8d6348f09bCAS |
Young TE, Gallie DR, Demason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiology 115, 737–751.
| Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntFSlsL0%3D&md5=e050121b75b5a8b2003a73d3bd2c21fcCAS |
Zhou YF, Liu WZ (2011) Laticiferous canal formation in fruits of Decaisnea fargesii: a programmed cell death process? Protoplasma 248, 683–694.
| Laticiferous canal formation in fruits of Decaisnea fargesii: a programmed cell death process?Crossref | GoogleScholarGoogle Scholar |
Zhou YF, Shi HY, Liu WZ (2012) Ontogenesis of trichome-like cavities in Dictamnus dasycarpus. Flora – Morphology, Distribution, Functional Ecology of Plants 207, 63–73.
| Ontogenesis of trichome-like cavities in Dictamnus dasycarpus.Crossref | GoogleScholarGoogle Scholar |
Zhou YF, Mao SL, Li SF, Ni XL, Li B, Liu WZ (2014) Programmed cell death: a mechanism for the lysigenous formation of secretory cavities in leaves of Dictamnus dasycarpus. Plant Science 225, 147–160.
| Programmed cell death: a mechanism for the lysigenous formation of secretory cavities in leaves of Dictamnus dasycarpus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFGqs7zP&md5=273abaa17d774f84baddf660f4435d82CAS |
