摘要
细胞程序性死亡(programmed cell death, PCD)是指受到严格控制并且主动有序的细胞死亡。这一过程对于机体防御反应,限制病原菌扩散以及多细胞生物个体的正常生长发育至关重要。
PDCD5 (programmed cell death 5)基因参与细胞程序性死亡的调控并且在进化过程中非常保守。OsPDCD5基因是我们通过水稻分化和未分化的愈伤组织间的抑制消减杂交(SSH)分离得到PDCD5的同源基因。在之前的研究中,我们发现组成型过表达OsPDCD5的水稻转基因再生植株直到三叶期才逐渐死亡,为了研究其原因是因为转基因植株的OsPDCD5表达量在三叶期前不足以诱导细胞死亡,还是因为幼嫩的植株具有某种可以抑制细胞死亡的机制,我们构建了一个可以通过热激来诱导OsPDCD5表达的系统。
从细菌到人类都具有合成热激蛋白(HSPs)的能力,它们在有机体受到高温胁迫(热激)时大量表达。Oshsp 16.9C (Accession No. U81385)是一种水稻|型低分子量HSP基因,它在28℃时基本没有转录,但在41℃热激诱导2小时后转录水平显著增加。将Oshsp 16.9C启动子驱动的OsPDCD5转化籼稻品种"9311”和粳稻品种“中花11”,所获得的转基因植株在28℃时可以正常生长,但在生长发育的任何阶段都可以通过41℃热激处理来诱导OsPDCD5的表达,使得我们可以对其诱导的细胞死亡进行详细的系统研究。结果表明OsPDCD5只能在三叶期及以后的植株中诱导细胞死亡,植株表现出生成枯斑,叶片枯萎,DNA片断化,产生过氧化物以及线粒体膨胀等症状。芯片结果显示很多PCD相关基因的转录水平都明显改变,其中包括Bcl-2-associated athanogene (BAG)家族基因以及可以在酵母和拟南芥中诱导PCD的AtBAG6的同源基因。但是OsPDCD5在二叶期及以前的植株中却不能诱导细胞死亡,并且没有导致任何症状。芯片结果和实时定量PCR的结果表明Bax inhibitor-1基因和一个ubiquitin基因与此现象密切相关,表明幼嫩植株确实拥有抑制OsPDCD5诱导的细胞死亡的机制。综合之前的结果和本次的实验数据,我们推测OsPDCD5可能通过影响钙离子平衡继而导致线粒体功能障碍这一途径来参与PCD通路的调控。
OsPDCD5具有重要的实际应用价值：在非光敏的籼稻品种金23B中反义表达OsPDCD5,转基因植株的抽穗期推迟,叶片衰老延缓,产量明显提高；OsPDCD5的诱导表达系统可以用于无标记转基因株系的获取。
棉花是一种重要的经济作物,它是天然纤维的主要来源,还是重要的油料作物。棉花有八千年的种植历史,是世界经济的重要组成部分。提高棉纤维的产量和品质是棉花育种的主要目标。棉纤维更准确地生物学名称是毛状体,因为它们是从胚珠表皮生成的,并不属于维管组织。虽然大多数植物的毛状体都是多细胞结构,棉纤维却是由单细胞构成的。由于棉纤维高度伸长,因此它的长度在一定程度上可以直接反映细胞的大小。棉纤维的长度对纱线的强度和均匀度以及纺纱的效率都有影响。因此,棉纤维的长度在影响棉花产量的同时,还影响棉花的品质。单细胞棉纤维的长度和受稳态调控的细胞大小直接相关,主要由基因型决定。
在之前的研究中,我们发现水稻开花控制基因FCA的RNA recognition motif (RRM)FCA-RRM1和FCA-RRM2的过表达都具有增大细胞大小和提高产量的功能,这说明FCA-RRM1和FCA-RRM2可能参与细胞大小的调控。同时,它们在进化中都表现出了高度的保守性,暗示FCA-RRM2在不同植物中可能具有相似的功能。在油菜中过表达油菜FCA-RRM2(Bn-csRRM2)基因的结果证明了这一推论(未发表)。为了验证B门一csRRM2的跨种保守性,我们又将其用于转化棉花,结果显示Bn-csRRM2在棉花中也能起作用,暗示csRRM2可能是一个古老且普遍的细胞大小调控因子。虽然csRRM2调控细胞大小的机制尚未明了,但是它提供了一条解决细胞大小问题的途径,同时还使得转基因棉花的品质和产量显著提高,具有重大的经济价值。由于csRRM2氨基酸序列的高度保守性,我们推测它可能在小麦,杨树和l蓖麻等植物中也起到增加产量的作用。
Programmed cell death (PCD) has been defined as a sequence of events that lead to the controlled and organized destruction of a cell. This process is crucial for organismal defense responses, to restrict the spread of pathogens, and for proper development of a multicellular body plan.
OsPDCD5 is a homolog gene of PDCD5, which is involved in PCD regulation and conserved in the course of evolution. In our previous research, constitutive overexpression of OsPDCD5 proved to induce plant death in rice, but none of the regenerated transgenic plant died until 3-leaf stage.
Why OsPDCD5did not effect in younger plants? Is there not enough amount of OsPDCD5transcripts until 3-leaf stageor there are some mechanisms which prevent OsPDCD5 function in younger plants? To resolve this problem, a system of inducible OsPDCD5 expression is required. Heat shock proteins (HSPs) have been detected during thermal stress in all organisms examined, ranging from bacteria to human beings. The heat inducible expression of HSPs results from the heat inducible transcription of HSP gene promoters. Oshsp 16.9C(Accession No. U81385) is a kind of rice class I low-molecular-mass HSP gene that is barely transcribed at 28℃, but the concentration of Oshsp 16.9C mRNA increases significantly in rice heat-shocked at 41℃for 2 h. In this work,Oshsp 16.9C promoter-driven OsPDCD5was used for the transformation of japonica rice Zhonghua 11 and indica rice 9311. The resulting transgenic plants grew normally at 28℃and OsPDCD5 transcription could be induced at any developmental stage by heat shockat 41℃, which allowed detailed, systematic study of OsPDCD5 induced rice cell death.The results showed that in 3-leaf stage and older seedlings, ectopic OsPDCD5 expression could independently induce cell death. In altered plants, OsPDCD5 expression caused a lesion mimic phenotype, abnormal leaf morphology, DNA fragmentation, H2O2 production, and mitochondrial distortion. Transcript microarray analysis revealed that many PCD-related genes were involved, including Bcl-2-associated athanogene (BAG) family genes and a homolog gene of AtBAG6, which can induce PCD in yeast and the Arabidopsis plant. Nevertheless, ectopic OsPDCD5 expression failed to induce any visibly morphological phenotype in 2-leaf stage and younger seedlings. At the same time, transcript microarray analysis and quantitative RT-PCR showed the mRNA level of a Bax inhibitor-1 gene and an ubiquitin gene changed, suggesting young seedlings possess some mechanisms which inhibit this OsPDCD5-induced cell death. These findings strongly suggest that the OsPDCD5 gene critically regulates the execution of PCD and calcium induced mitochondrial dysfunction may play an important role in this pathway.
The antisense-OsPDCD5 transgenic J23B plants demonstrate a delay of heading date and leaf senescence, leading to a great increase on grain yield. Furthermore,the OsPDCD5 inducible expression system can be used to regenerate marker-free transgenic plants by co-transformation, indicating OsPDCD5is of great practical application value.
Cotton (Gossypium hirsutum L.) is the dominant source of natural textile fiber and a significant oil crop and has been a valued agricultural commodity for more than 8000 years. Many cotton improvement programs have been established to improve this crop. The key goals are to improve the yield and the quality of the fiber. The appropriate botanically term for cotton fiber is trichome, which is developed from the ovule epidermis and is not part of the vascular tissue. While the majority of plant trichomes are multicellular, cotton trichome cells are unicellular. As cotton fiber cell is highly elongated, its length basically represents its size. Cotton fiber length affects yarn strength, yarn evenness, and spinning efficiency. Thus, thelengthof cotton trichome cell not only affects yield but also cotton quality. The average length of unicellular cotton fibers varies with genotype and is apparently under homeostatic control. However, not much is known about the underlying aspect of the control. Thus, information that can shed light on the control could be useful for improving cotton fiber yield and quality.
We have previously found that cell size and yield of rice (Oryza sativa) can be increased by overexpression of RNA recognition motif (RRM) FCA-RRM1, as well as FCA-RRM2, of the rice flowering control gene FCA (6,7). This suggests that FCA-RRM1 and FCA-RRM2 both play a role in homeostatic cell size regulation. Both FCA-RRMs exhibit a high degree of evolutionary conservation in plant. The high degree of homology suggests that this RRM domain might have similar function in different plants. Indeed, we observed that overexpression of Brassica napusFCA-RRM2 (Bn-csRRM2) also increased the cell size of B. napus (unpublished data).In order to validate the inter-species effect of Bn-csRRM2 function, cotton (Gossypium hirsutum) was used for transformation. The results showed that Bn-csRRM2 even worked in cotton, suggesting csRRM2 might be an ancient and common cell size regulator.Although the mechanism by which csRRM2 influences cell size regulation is still unclear, csRRM2 offers a potential way to resolve this problem. Besides its biological significance, csRRM2 also has great economic value and considerable influence on cotton industry because it leads to visible increase on both fiber quality and fiber yield which are exceedingly difficult to incorporate into a single breeding program. Thinking of the high conservation of csRRM2, it may also work in other crops, such as Triticum aestivum, Populus trichocarpa and Ricinus communis.
引文
Abramovitch, R. B. Type Ⅲ effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity [J]. Proceedings of the National Academy of Sciences,2006, 103(8):2851-2856.
Apel, K. and H. Hirt. Reactive oxygen species:metabolism, oxidative stress, and signal transduction [J]. Annual Review of Plant Biology,2004, 55:373-399.
Arpagaus, S., A. Rawyler, et al. Occurrence and characteristics of the mitochondrial permeability transition in plants [J]. Journal of Biological Chemistry,2002,277(3):1780-1787.
Arpat, A., M. Waugh, et al. Functional genomics of cell elongation in developing cotton fibers [J]. Plant molecular biology,2004, 54(6):911-929.
Attia, K., L. Ke-Gui, et al. Overexpression of the OsPDCD5 gene induces programmed cell death in rice [J]. Journal of Integrative Plant Biology, 2005,47(9):1115-1122.
Attia, K., K. Li, et al. Transformation and functional expression of the rFCA-RRM2 gene in rice [J]. Journal of Integrative Plant Biology,2005, 47(7):823-830.
Balk, J., S. Chew, et al. The intermembrane space of plant mitochondria contains a DNase activity that may be involved in programmed cell death [J]. The Plant Journal,2003,34(5):573-583.
Balk, J. and C. Leaver. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release [J]. The Plant Cell,2001,13(8):1803-1818.
Baurle, I., L. Smith, et al. Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing [J]. Science,2007, 318(5847):109-112.
Birney, E., S. Kumar, et al. Analysis of the RNA-recognition motif and RS and RGG domains:conservation in metazoan pre-mRNA splicing factors [J]. Nucleic Acids Research,1993,21(25):5803.
Bonneau, L., Y. Ge, et al. What happened to plant caspases? [J]. Journal of Experimental Botany,2008.
Bowen, I., S. Morgan, et al. Cell death in the salivary glands of metamorphosing Calliphora vomitoria [J]. Cell biology international, 1993,17(1):13-34.
Broadhurst, M., R. Lee, et al. The p100 EBNA-2 coactivator:a highly conserved protein found in a range of exocrine and endocrine cells and tissues in cattle [J]. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression,2005,1681(2-3):126-133.
Burbridge, E., M. Diamond, et al. Use of cell morphology to evaluate the effect of a peroxidase gene on cell death induction thresholds in tobacco [J]. Plant Science,2006,171(1):139-146.
Burd, C. and G. Dreyfuss. Conserved structures and diversity of functions of RNA-binding proteins [J]. Science,1994,265(5172):615.
Chen, G., L. Huang, et al. Molecular characterization of a senescence-associated gene encoding cysteine proteinase and its gene expression during leaf senescence in sweet potato [J]. Plant and cell physiology,2002,43(9):984.
Chen, Y., R. Sun, et al. Nuclear translocation of PDCD5 (TFAR19):an early signal for apoptosis? [J]. FEBS letters,2001,509(2):191-196.
Clarke, A., R. Desikan, et al. NO way back:nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures [J]. The Plant Journal, 2000,24(5):667-677.
Clouse, S. Molecular genetic studies confirm the role of brassinosteroids in plant growth and development [J]. The Plant Journal,1996,10(1):1-8.
Coffeen, W. and T. Wolpert. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa [J]. The Plant Cell Online,2004, 16(4):857.
Cregg, J. and K. Madden. Use of site-specific recombination to regenerate selectable markers [J]. Molecular and General Genetics MGG,1989, 219(1):320-323.
Dat, J., R. Pellinen, et al. Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco [J]. The Plant Journal,2003, 33(4):621-632.
De Jong, A., F. Hoeberichts, et al. Chemical-induced apoptotic cell death in tomato cells:involvement of caspase-like proteases [J]. Planta,2000, 211(5):656-662.
del Pozo, O. and E. Lam. Caspases and programmed cell death in the hypersensitive response of plants to pathogens [J]. Current Biology, 1998,8(20):1129-1132.
Demao, J., L. Xia, et al. The characteristics of CO2 assimilation of photosynthesis and chlorophyll fluorescence in transgenic PEPC rice [J]. Chinese Science Bulletin,2001,46(13):1080-1084.
Demaurex, N. and C. Distelhorst. CELL BIOLOGY:Apoptosis-the Calcium Connection [J]. Science Signaling,2003,300(5616):65-67.
Dion, M., H. Chamberland, et al. Detection of a homologue of bcl-2 in plant cells [J]. Biochemistry and Cell Biology,1997,75(4):457-461.
Doke, N. and Y. Ohashi. Involvement of an O2-generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus [J]. Physiological and Molecular plant pathology,1988, 32(1):163-175.
Dreyfuss, G., M. Matunis, et al. hnRNP proteins and the biogenesis of mRNA [J]. Annual review of biochemistry,1993,62(1):289-321.
Earnshaw, W., L. Martins, et al. Mammalian caspases:structure, activation, substrates, and functions during apoptosis [J]. Annual review of biochemistry,1999,68(1):383-424.
Ebinuma, H., K. Sugita, et al. Systems for the removal of a selection marker and their combination with a positive marker [J]. Plant Cell Reports, 2001,20(5):383-392.
Ebinuma, H., K. Sugita, et al. Selection of marker-free transgenic plants using the isopentenyl transferase gene [J]. Proceedings of the National Academy of Sciences of the United States of America,1997, 94(6):2117.
Fantes, P. Control of cell size and cycle time in Schizosaccharomyces pombe [J]. Journal of cell science,1977,24(1):51-67.
Ferri, K. and G. Kroemer. Organelle-specific initiation of cell death pathways [J]. Nature cell biology,2001,3(11):E255-E263.
Frary, A., T. Nesbitt, et al. fw2.2:a quantitative trait locus key to the evolution of tomato fruit size [J]. Science,2000,289(5476):85-88.
Fu, Y., Y. Ding, et al. Rice transformation with a senescence-inhibition chimeric gene [J]. Chinese Science Bulletin,1998,43(21):1810-1815.
Gan, S. and R. Amasino. Making sense of senescence:molecular genetic regulation and manipulation of leaf senescence [J]. Plant Physiology, 1997,113(2):313-319.
Gechev, T. and J. Hille. Hydrogen peroxide as a signal controlling plant programmed cell death [J]. Journal of Cell Biology,2005,168(1):17-20.
Gleave, A., D. Mitra, et al. Selectable marker-free transgenic plants without sexual crossing:transient expression of cre recombinase and use of a conditional lethal dominant gene [J]. Plant molecular biology,1999, 40(2):223-235.
Green, D. and G. Kroemer. The pathophysiology of mitochondrial cell death[J]. Science,2004,305(5684):626-629.
Greenberg, J. Programmed cell death:a way of life for plants [J]. Proceedings of the National Academy of Sciences of the United States of America, 1996,93(22):12094.
Greenberg, J., A. Guo, et al. Programmed cell death in plants:a pathogen-triggered response activated coordinately with multiple defense functions [J]. Cell,1994,77(4):551-563.
Guo-Yin, K., Z. Lei, et al. Marker-free:a novel tendency of transgenic plants [J]. Acta Botanica Sinica,2002,44(8):883-888.
Hatsugai, N., M. Kuroyanagi, et al. A cellular suicide strategy of plants: vacuole-mediated cell death [J]. Apoptosis,2006,11(6):905-911.
Hatsugai, N., M. Kuroyanagi, et al. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death [J]. Science,2004, 305(5685):855.
Heath, M. Hypersensitive response-related death [J]. Plant molecular biology, 2000,44(3):321-334.
Hetz, C. ER stress signaling and the BCL-2 family of proteins:from adaptation to irreversible cellular damage [J]. Antioxidants & Redox Signaling, 2007,9(12):2345-2356.
Hoeberichts, F., A. Have, et al. A tomato metacaspase gene is upregulated during programmed cell death in Botrytis cinerea-infected leaves [J]. Planta,2003,217(3):517-522.
Hohn, B., A. Levy, et al. Elimination of selection markers from transgenic plants [J]. Current Opinion in Biotechnology,2001,12(2):139-143.
Hong, F., K. Attia, et al. Overexpression of the r FCA RNA Recognition Motif Affects Morphologies Modifications in Rice (Oryza sativa L.) [J]. Bioscience Reports,2007,27(4):225-234.
Huang, L., Q. Sun, et al. Down-regulation of a SILENT INFORMATION REGULATOR2-related histone deacetylase gene, OsSRT1, induces DNA fragmentation and cell death in rice [J]. Plant Physiology,2007, 144(3):1508-1519.
Huang, P. and W. Plunkett. A quantitative assay for fragmented DNA in apoptotic cells [J]. Analytical biochemistry,1992,207(1):163-167.
Hubbard, L., P. McSteen, et al. Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte [J]. Genetics,2002,162(4):1927.
Ihara-Ohori, Y., M. Nagano, et al. Cell death suppressor Arabidopsis bax inhibitor-1 is associated with calmodulin binding and ion homeostasis [J]. Plant Physiology,2007,143(2):650-660.
Jabs, T. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals [J]. Biochemical Pharmacology,1999, 57(3):231-245.
Jesenberger, V. and S. Jentsch. Deadly encounter:ubiquitin meets apoptosis [J]. Nature Reviews Molecular Cell Biology,2002,3(2):112-121.
Jiang, C., S. Rodermel, et al. Photosynthesis, Rubisco activity and amount, and their regulation by transcription in senescing soybean leaves [J]. Plant Physiology,1993,101(1):105.
Jofuku, K., P. Omidyar, et al. Control of seed mass and seed yield by the floral homeotic gene APETALA2 [J]. Proceedings of the National Academy of Sciences,2005,102(8):3117-3122.
Jones, A. Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? [J]. Trends in Plant Science,2000, 5(5):225-230.
Kang, C., W. Jung, et al. AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants [J]. Cell Death and Differentiation 2005,13:84-95.
Kawai-Yamada, M., L. Jin, et al. Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax lnhibitor-1 (AtBI-1) [J]. Proceedings of the National Academy of Sciences,2001, 98(21):12295-12300.
Kawai, M., L. Pan, et al. Evolutionally conserved plant homologue of the Bax inhibitor-1 (BI-1) gene capable of suppressing Bax-induced cell death in yeast [J]. FEBS letters,1999,464(3):143-147.
Kawanabe, T., T. Ariizumi, et al. Abolition of the tapetum suicide program ruins microsporogenesis [J]. Plant and cell physiology,2006,47(6):784-787.
Kim, H. and B. Triplett. Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis [J]. Plant Physiology,2001, 127(4):1361-1366.
Kim, M., J. Lim, et al. Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana [J]. The Plant Cell,2006,18(9):2341-2355.
Kim, R., M. Emi, et al. Role of mitochondria as the gardens of cell death [J]. Cancer chemotherapy and pharmacology,2006,57(5):545-553.
Klionsky, D. and S. Emr. Autophagy as a regulated pathway of cellular degradation [J]. Science,2000,290(5497):1717.
Komari, T., Y. Hiei, et al. Vectors carrying two separate T-DNAs for co-transformation of higher plants mediated by Agrobacterium tumefaciens and segregation of transformants free from selection markers [J]. The Plant Journal,1996,10(1):165-174.
Kowaltowski, A., R. Castilho, et al. Mitochondrial permeability transition and oxidative stress [J]. FEBS letters,2001,495(1-2):12-15.
Kuroyanagi, M., M. Nishimura, et al. Activation of Arabidopsis vacuolar processing enzyme by self-catalytic removal of an auto-inhibitory domain of the C-terminal propeptide [J]. Plant and cell physiology,2002, 43(2):143.
Lacomme, C. and S. Santa Cruz. Bax-induced cell death in tobacco is similar to the hypersensitive response [J]. Proceedings of the National Academy of Sciences of the United States of America,1999, 96(14):7956.
Lam, E. Controlled cell death, plant survival and development [J]. Nature Reviews Molecular Cell Biology,2004,5(4):305-315.
Lam, E. and O. Pozo. Caspase-like protease involvement in the control of plant cell death [J]. Plant molecular biology,2000,44(3):417-428.
Leshem, Y. Plant senescence processes and free radicals [J]. Free Radical Biology and Medicine,1988,5(1):39-49.
Li, P., D. Nijhawan, et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade [J]. Cell,1997,91(4):479-489.
Li, S., D. Yin, et al. Introduction of the PPF1 gene into rice (Oryza sativa L.) results in delayed leaf senescence [J]. Euphytica,2007, 153(1):257-265.
Li, T., Y. Tian, et al. Transgenic tobacco plants with efficient insect resistance [J]. Science in China Series B. Chemistry, Life Sciences & Earth Sciences,1994,37(12):1479-1488.
Liu, H., Y. Wang, et al. TFAR19, a novel apoptosis-related gene cloned from human leukemia cell line TF-1, could enhance apoptosis of some tumor cells induced by growth factor withdrawal [J]. Biochemical and Biophysical Research Communications,1999,254(1):203-210.
Lohman, K., S. Gan, et al. Molecular analysis of natural leaf senescence in Arabidopsis thaliana [J]. Physiologia Plantarum,1994,92(2):322-328.
Mach, J., A. Castillo, et al. The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms [J]. Proceedings of the National Academy of Sciences of the United States of America,2001,98(2):771.
Macknight, R., I. Bancroft, et al. FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains [J]. Cell,1997,89(5):737-745.
Macknight, R., M. Duroux, et al. Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA [J]. The Plant Cell,2002,14(4):877-888.
Madeo, F., E. Herker, et al. A caspase-related protease regulates apoptosis in yeast [J]. Molecular Cell,2002,9(4):911-917.
Mariani, C., V. Gossele, et al. A chimaeric ribonuclease-inhibitor gene restores fertility to male sterile plants [J]. Nature,1992,357(6377):384-387.
Maris, C., C. Dominguez, et al. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression [J]. FEBS Journal,2005,272(9):2118-2131.
Marty, F. Plant vacuoles [J]. The Plant Cell,1999,11(4):587.
McCabe, P. Apoptotic-like programmed cell death in plants [J]. New Phytologist,2008,180(1):13-26.
Michaels, S. and R. Amasino. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering [J]. The Plant Cell, 1999,11(5):949.
Michaels, S. and R. Amasino. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization [J]. The Plant Cell,2001,13(4):935.
Mignotte, B. and J. Vayssiere. Mitochondria and apoptosis [J]. European Journal of Biochemistry,1998,252(1):1-15.
Mitsuhara, I., K. Malik, et al. Animal cell-death suppressors Bcl-xL and Ced-9 inhibit cell death in tobacco plants [J]. Current Biology,1999, 9(14):775-778.
Nagano, M., Y. lhara-Ohori, et al. Functional association of cell death suppressor, Arabidopsis Bax inhibitor-1, with fatty acid 2-hydroxylation through cytochrome b5 [J]. The Plant Journal,2009,58(1):122-134.
Neill, S., R. Desikan, et al. Hydrogen peroxide and nitric oxide as signalling molecules in plants [J]. Journal of Experimental Botany,2002, 53(372):1237.
Onouchi, H., R. Nishihama, et al. Visualization of site-specific recombination catalyzed by a recombinase from Zygosaccharomyces rouxii in Arabidopsis thaliana [J]. Molecular and General Genetics MGG,1995, 247(6):653-660.
Panda, S., Y. Yamamoto, et al. Mitochondrial alterations related to programmed cell death in tobacco cells under aluminium stress [J]. Comptes rendus-Biologies,2008,331(8):597-610.
Papini, A., S. Mosti, et al. Programmed-cell-death events during tapetum development of angiosperms [J]. Protoplasma,1999,207(3):213-221.
Qian, Y. Analysis of advantages and disadvantages on transgenic crops [J]. Biotechnology Information,1999,5:7-11.
Quesada, V., R. Macknight, et al. Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time [J]. The EMBO Journal,2003, 22(12):3142.
Reape, T., E. Molony, et al. Programmed cell death in plants:distinguishing between different modes [J]. Journal of Experimental Botany,2008, 59(3):435-444.
Reape, T. J. and P. F. McCabe. Apoptotic-like regulation of programmed cell death in plants [J]. Apoptosis,2010,15(3):249-256.
Reed, J. Double identity for proteins of the Bcl-2 family [J]. Nature,1997, 387(6635):773-776.
Rojo, E. VPE gamma exhibits a caspase-like activity that contributes to defense against pathogens [J]. Current Biology,2004, 14(21):1897-1906.
Rojo, E., J. Zouhar, et al. A unique mechanism for protein processing and degradation in Arabidopsis thaliana [J]. Proceedings of the National Academy of Sciences of the United States of America,2003, 100(12):7389.
Rotari, V., R. He, et al. Death by proteases in plants:whodunit [J]. Physiologia Plantarum,2005,123(4):376-385.
Ryerson, D. and M. Heath. Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments [J]. The Plant Cell,1996,8(3):393.
Sanmartin, M., L. Jaroszewski, et al. Caspases. Regulating death since the origin of life [J]. Plant Physiology,2005,137(3):841.
Scandalios, J. Oxygen stress and superoxide dismutases [J]. Plant Physiology, 1993,101(1):7.
Scorrano, L. and S. Korsmeyer. Mechanisms of cytochrome c release by proapoptotic BCL-2 family members [J]. Biochemical and Biophysical Research Communications,2003,304(3):437-444.
Shi, Y. Mechanisms of caspase activation and inhibition during apoptosis [J]. Molecular Cell,2002,9(3):459-470.
Shirahama-Noda, K., A. Yamamoto, et al. Biosynthetic processing of cathepsins and lysosomal degradation are abolished in asparaginyl endopeptidase-deficient mice [J]. Journal of Biological Chemistry,2003, 278(35):33194.
Simpson, G., P. Dijkwel, et al. FY is an RNA 3' end-processing factor that interacts with FCA to control the Arabidopsis floral transition [J]. Cell, 2003,113(6):777-787.
Su, W., J. Wu, et al. Interaction between programmed cell death 5 and calcineurin B-like interacting protein kinase 23 in Oryza sativa [J]. Plant Science,2006,170(6):1150-1155.
Suarez, M., L. Filonova, et al. Metacaspase-dependent programmed cell death is essential for plant embryogenesis [J]. Current biology,2004, 14(9):R339.
Sun, Y., Y. Zhao, et al. Cytochrome c release and caspase activation during menadione-induced apoptosis in plants [J]. FEBS letters,1999, 462(3):317-321.
Sundstr m, J., A. Vaculova, et al. Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome [J]. Nature cell biology,2009.
Susin, S., N. Zamzami, et al. Mitochondria as regulators of apoptosis:doubt no more [J]. Biochimica et Biophysica Acta (BBA)-Bioenergetics,1998, 1366(1-2):151-165.
Thomas, H. and C. Howarth. Five ways to stay green [J]. Journal of Experimental Botany,2000,51 (Special Issue):329.
Thomas, H. and C. Smart. Crops that stay green [J]. Annals of Applied Biology, 1993,123(1):193-219.
Thompson, A. and R. Vierstra. Autophagic recycling:lessons from yeast help define the process in plants [J]. Current opinion in plant biology,2005, 8(2):165-173.
Tian, R., G. Zhang, et al. Involvement of poly (ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells [J]. FEBS letters,2000,474(1):11.
Tiwari, B., B. Belenghi, et al. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death [J]. Plant Physiology,2002,128(4):1271-1281.
Vacca, R., D. Valenti, et al. Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco Bright-Yellow 2 cells en route to heat shock-induced cell death [J]. Plant Physiology,2006,141(1):208.
van Doom, W. and E. Woltering. Many ways to exit? Cell death categories in plants [J]. Trends in Plant Science,2005,10(3):117-122.
Vaux, D. Caspases and apoptosis-biology and terminology [J]. Cell Death and Differentiation,1999,6(6):493.
Vaux, D. and S. Korsmeyer. Cell death in development [J]. Cell,1999, 96(2):245-254.
Vernon, D., M. Hannon, et al. An expanded role for the TWN1 gene in embryogenesis:defects in cotyledon pattern and morphology in the twn1 mutant of Arabidopsis (Brassicaceae) [J]. American Journal of Botany,2001,88(4):570.
Vernon, D. and D. Meinke. Embryogenic transformation of the suspensor in twin, a polyembryonic mutant of Arabidopsis [J]. Developmental biology, 1994,165(2):566-573.
Virolainen, E., O. Blokhina, et al. Ca2+-induced high amplitude swelling and cytochrome c release from wheat (Triticum aestivum L.) mitochondria under anoxic stress [J]. Annals of Botany,2002,90(4):509-516.
Wang, C. and D. Klionsky. The molecular mechanism of autophagy [J]. Molecular Medicine,2003,9(3-4):65.
Wang, X. The expanding role of mitochondria in apoptosis [J]. Genes & development,2001,15(22):2922-2933.
Wang, Y., X. Li, et al. An alternative form of paraptosis-like cell death, triggered by TAJ/TROY and enhanced by PDCD5 overexpression [J]. Journal of cell science,2004,117(8):1525-1532.
Wang, Y., X. Zha, et al. Down-regulation of the OsPDCD5 gene induced photoperiod-sensitive male sterility in rice [J]. Plant Science,2010, 178(2):221-228.
Watanabe, N. and E. Lam. Recent advance in the study of caspase-like proteases and Bax inhibitor-1 in plants:their possible roles as regulator of programmed cell death [J]. Molecular Plant Pathology,2004, 5(1):65-70.
Watanabe, N. and E. Lam. BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis [J]. Journal of Biological Chemistry,2008,283(6):3200-3210.
Watanabe, N. and E. Lam. Bax inhibitor-1, a conserved cell death suppressor, is a key molecular switch downstream from a variety of biotic and abiotic stress signals in plants [J]. International Journal of Molecular Sciences,2009,10(7):3149-3167.
Westoby, M., M. Leishman, et al. Comparative Ecology of Seed Size and Dispersal [and Discussion] [J]. Philosophical Transactions:Biological Sciences,1996,351 (1345):1309-1318.
Woltering, E. Death proteases come alive [J]. Trends in Plant Science,2004, 9(10):469-472.
Woltering, E. Death proteases:alive and kicking [J]. Trends in Plant Science, 2010,15(4):185-188.
Wu, H. and A. Cheung. Programmed cell death in plant reproduction [J]. Plant molecular biology,2000,44(3):267-281.
Wyllie, A. Apoptosis:an overview [J]. British Medical Bulletin,1997,53(3):451.
Xu, F. and M. Chye. Expression of cysteine proteinase during developmental events associated with programmed cell death in brinjal [J]. The Plant Journal,1999,17(3):321-327.
Xu, L., Y. Chen, et al. PDCD5 Interacts with Tip60 and Functions as a Cooperator in Acetyltransferase Activity and DNA Damage-Induced Apoptosis [J]. Neoplasia,2009,11(4):345-354.
Xu, Q. and J. Reed. Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast [J]. Molecular Cell,1998, 1(3):337-346.
Yang, C. W. The E3 Ubiquitin Ligase Activity of Arabidopsis PLANT U-BOX17 and Its Functional Tobacco Homolog ACRE276 Are Required for Cell Death and Defense [J]. The Plant Cell,2006,18(4):1084-1098.
Yang, Y. and X. Yu. Regulation of apoptosis:the ubiquitous way [J]. The FASEB Journal,2003,17(8):790-799.
Yi, K., B. Menand, et al. A basic helix-loop-helix transcription factor controls cell growth and size in root hairs [J]. Nature Genetics,2010, 42(3):264-267.
Zeng, L. R. Spotted leaf11, a Negative Regulator of Plant Cell Death and Defense, Encodes a U-Box/Armadillo Repeat Protein Endowed with E3 Ubiquitin Ligase Activity [J]. The Plant Cell,2004,16(10):2795-2808.