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Revista Mexicana de Fitopatologa

ISSN: 0185-3309
mrlegarreta@prodigy.net.mx
Sociedad Mexicana de Fitopatologa, A.C.
Mxico

Sanzn Gmez, Diana; Zavaleta Meja, Emma


Respuesta de Hipersensibilidad, una Muerte Celular Programada para Defenderse del Ataque por
Fitopatgenos
Revista Mexicana de Fitopatologa, vol. 29, nm. 2, 2011, pp. 154-164
Sociedad Mexicana de Fitopatologa, A.C.
Texcoco, Mxico

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154/VOLUMEN 29, NMERO 2, 2011

Respuesta de Hipersensibilidad, una Muerte Celular


Programada para Defenderse del Ataque por Fitopatgenos
Hypersensitive Reaction, a Programmed Cell Death to Defend from
Attack by Plant Pathogens
Diana Sanzn Gmez y Emma Zavaleta Meja, Instituto de Fitosanidad, Colegio de Postgraduados,
Km. 36.5 Carr. Mxico-Texcoco, Montecillo, Edo. de Mxico, CP 56230, Mxico. Correspondencia:
zavaleta@colpos.mx

(Recibido: Junio 21, 2010 Aceptado: Junio 14, 2011)

Sanzn GD y Zavaleta ME. 2011. Respuesta de Abstract. Programmed cell death (PCD) or cellular
Hipersensibilidad, una muerte celular programada para suicide occurs in all organisms as a normal process that
defenderse del ataque por fitopatgenos. Revista Mexicana takes place in an organized and perfectly regulated way,
de Fitopatologa 29:154-164. which is essential for the development and survival of the
organisms and it is also expressed in response to biotic or
Resumen. La muerte celular programada (MCP) o abiotic stresses in animals, plants and unicellular organisms.
suicidio celular, ocurre en los seres vivos como un proceso The PCD is a genetically controlled cell death which
normal que tiene lugar de una manera perfectamente requires an active participation of the organism and involves
organizada y regulada, que es fundamental para su a sequence of cellular metabolic events that lead to the
desarrollo y supervivencia, y que tambin se dispara en destruction of the cell. Currently, based upon the
respuestas a estrs por factores biticos o abiticos en morphological characteristics that the dying cells display
animales, plantas y en organismos unicelulares. La MCP es and in the kind of cellular organelle involved, three
un fallecimiento genticamente controlado, que requiere de categories of PCD death have been defined: apoptosis,
una participacin activa del organismo e involucra una lysosomal death or autophagy ('self-eating'), and non-
secuencia de eventos metablicos celulares que conducen a lysosomal death. The hypersensitive reaction (HR) is
la destruccin de la clula. Actualmente con base en las considered the maximum expression of plant resistance to
caractersticas morfolgicas que presentan las clulas que pathogen attack and is defined as a fast death of the plant
fallecen y en el tipo de organelo celular involucrado se han cells associated with the restriction of the pathogen growth,
definido tres categoras de MCP: apoptosis, muerte which usually is recognized by the presence of one or
lisosomal o autofagia, y muerte no lisosomal. La reaccin de several brown-colored dead cells at the infection site. The
hipersensibilidad (RH) es considerada como la mxima death of cells that happens during the HR is considered a
expresin de resistencia de las plantas al ataque por lysosomal type PCD or autophagy.
patgenos y se define como una muerte rpida de las clulas
vegetales asociada con la restriccin del crecimiento del
Additional keywords: Plant defense mechanisms,
patgeno, que generalmente se reconoce por la presencia de
compatible and incompatible plant-pathogen interactions,
una o varias clulas muertas con coloracin caf en el sitio
necrosis, plant resistance.
de infeccin. El fallecimiento de clulas que ocurre durante
la RH se considera una MCP de tipo lisosomal o autofagia. The hypersensitive reaction (HR) is considered the ultimate
expression of plant resistance to pathogen attack. During the
Palabras clave adicionales: Mecanismos de defensa en HR cells surround the site where the pathogen penetrated
plantas, interacciones planta-patgeno compatibles e and commit suicide with the intention of stopping its
incompatibles, necrosis, resistencia en plantas. progress and infection. Thus, the HR forms part of the plant's
defense mechanisms (Greenberg, 1997; Mur et al., 2008).
La reaccin de hipersensibilidad (RH) se considera como la The cell death that occurs during the HR is considered a
mxima expresin de resistencia de las plantas al ataque por Programmed Cell Death (PCD). Normally many of the cells
patgenos. Durante la RH las clulas que rodean el sitio of eukaryotic organisms die and are removed on a
donde penetr el patgeno se suicidan con la intencin de programmed basis through a series of sophisticated
detener su avance y la infeccin. As la RH forma parte de biochemical and morphological changes. PCD is
los mecanismos de defensa de la planta (Greenberg, 1997; fundamental in processes that are related to both growth and
Mur et al., 2008). El fallecimiento de clulas que ocurre normal development of the organism as a response to stress
durante la RH se considera una muerte celular programada caused by biotic and abioticfactors; it occurs in animals,
(MCP). Normalmente muchas de las clulas de los plants and unicellular organisms (Guimares and Linden,
REVISTA MEXICANA DE FITOPATOLOGA/155

organismos eucariontes mueren y son removidas de manera 2004; Williams and Dickman, 2008; Zandbergen et al.,
programada a travs de una serie de cambios bioqumicos y 2010). PCD is a genetically controlled death, which requires
morfolgicos sofisticados. La MCP es fundamental en the active participation of the organism (Greenberg, 1997;
procesos relacionados tanto con el crecimiento y desarrollo Williams and Dickman, 2008) and involves a sequence of
normal del organismo, como con la respuesta a estreses por metabolic events that lead to the destruction of the cell
factores biticos y abiticos; se presenta en animales, (Guimares and Linden, 2004; Williams and Dickman,
plantas y en organismos unicelulares (Guimares y Linden, 2008). It is suggested that animals and plants have
2004; Williams y Dickman, 2008; Zandbergen et al., 2010). conserved, at least in part, both cell death pathways and
La MCP es un fallecimiento genticamente controlado, que morphological characteristics through evolution (Ameisen,
requiere de una participacin activa del organismo 2002; Jimenez et al., 2009; Reape and McCabe, 2010;
(Greenberg, 1997; Williams y Dickman, 2008) e involucra Kaczanowski et al., 2011).
una secuencia de eventos metablicos que conducen a la Although most of the research work on PCD
destruccin de la clula (Guimares y Linden, 2004; mechanisms has been carried out in animals and relatively
Williams y Dickman, 2008). Se sugiere que a travs de la little has been investigated in plants, it has been documented
evolucin se han conservado en animales y plantas al menos that the cell death in plants has similarities with cell death in
parte, tanto de las rutas de la muerte celular, como de las animals. Previously, Camarena (2006) published in Mexico
caractersticas morfolgicas (Ameisen, 2002; Jimnez et a review on programmed cell death as a response to
al., 2009; Reape y McCabe, 2010; Kaczanowski et al., environmental stress, but it did not comprehensively address
2011). this type of PCD in plant-pathogen interactions.
Aunque la mayora de los trabajos de investigacin This review complements the studies made by
sobre los mecanismos de la MCP, se han llevado a cabo en Camarena (2006), by emphasizing on PCD that involves
animales y relativamente poco se ha investigado en plantas, hypersensitive cell death in the plant-pathogen interaction,
por ahora se ha documentado que la muerte celular en particularly with fungi, oomycetes and bacteria.
plantas presenta similitudes con la muerte celular en Furthermore, information from recent years on the
animales. Con anterioridad, Camarena (2006) public en morphological and ultrastructural changes experienced by
Mxico una revisin sobre muerte celular programada como cells in this type of cellular death are mentioned and
una respuesta al estrs ambiental, pero no aborda de manera highlighted, a topic scarcely discussed in other documents
amplia este tipo de MCP en la interaccin planta-patgeno. that emphasize the biochemical changes.
La presente revisin complementa la realizada por Programmed cell death in plants. The cells of
Camarena (2006), al enfatizar aquella que involucra la organisms can die from "suicide" or "murder" (Figure 1).
muerte celular hipersensitiva en la interaccin planta- The PCD is a cellular self-destruction (suicide) that
patgeno, particularmente con hongos, oomicetos y presents itself as a normal process in living organisms, that
bacterias. Adems, se menciona y se resalta la informacin takes place in a perfectly organized and regulated manner,
de los ltimos aos sobre los cambios morfolgicos y which is fundamental for development and survival, and that
ultraestructurales que sufren las clulas en este tipo de is also triggered in response to biotic and abiotic stress
muerte celular, tema poco abordado en otros documentos factors (Lakinova et al., 2005; Williams and Dickman,
que enfatizan los cambios bioqumicos. 2008; Zandbergen et al., 2010). In contrast with the PCD,
Muerte celular programada en plantas. Las necrosis in a figurative way is a murder in which the
clulas de los organismos pueden fallecer por suicidio o por cellular death results from the exposition to of toxic
asesinato (Figura 1). La MCP es una autodestruccin compounds, severe stress from heat or cold, or severe
(suicidio) celular que se presenta como un proceso normal damage that causes immediate and irreversile deterioration
en los seres vivos, que tiene lugar de una manera to membrane and cellular organelles (Reape et al., 2008;
perfectamente organizada y regulada, que es fundamental Williams and Dickman, 2008).
para su desarrollo y supervivencia, y que tambin se dispara In plants, cellular suicide or PCD, is present in
en respuestas a estrs por factores biticos o abiticos various stages of its development as a normal process of
(Lakimova et al., 2005; Williams y Dickman, 2008; differentiation of tissues and organs, and the adaptation to
Zandbergen et al., 2010). En contraste con la MCP, la environmental conditions; the evidence obtained in several
necrosis en un sentido figurado es un asesinato en el que la models, both in vitro and in vivo, support the hypothesis that
muerte celular resulta de la exposicin a compuestos a variety of PCD's may be triggered in different
txicos, estrs severo por fro o calor, o dao severo que circumstances (Guimares and Linden, 2004; Wang et al.,
causa un deterioro inmediato e irreversible a la membrana u 2010; Nakaba et al., 2011; Wang and Zhang, 2011) and
organelos celulares (Reape et al., 2008; Williams y consequently, there are differences in the morphological
Dickman, 2008). changes experienced by dying cells. Some examples of PCD
En plantas, el suicidio celular o MCP, se presenta en that commonly occur in plants are: 1) the degeneration of
varias etapas de su desarrollo como un proceso normal de specific cells that occur during the growth of the embryo and
diferenciacin de tejidos y rganos, y de adaptacin a germination (the suspensor cells of the embryo and or
condiciones ambientales; las evidencias obtenidas en varios endosperm die), the death of the cotyledons, petals, carpels
sistemas modelo, tanto in vitro como in vivo, soportan la and other floral parts, and the parenchymal cells in the
hiptesis de que una variedad de MCPs pueden ser formation of the aerenchyma; 2) the differentiation of male
156/VOLUMEN 29, NMERO 2, 2011

MUERTE CELULAR

AUTOFAGIA

MUERTE NO
APOPTOSIS ESTRS CELULAR O LISOSOMAL
DAO (NECROSIS
PROGRAMADA)

MUERTE CELULAR

NECROSIS

MUERTE CELULAR

Figura 1. Tipos de degeneracin celular que ocurren en clulas sujetas a estrs o dao. Los tipos de muerte celular programada
se indican en los rectngulos negros. El fallecimiento de la clula (muerte celular, indicada en los rectngulos con lneas
discontinuas) puede ocurrir por suicidio (muerte celular programada) o por asesinato (la muerte celular resulta de la exposicin
a compuestos txicos, estrs severo por fro o calor, o dao severo que causa un dao inmediato irreversible a la membrana u
organelos celulares).
Figure 1. Types of cell degeneration that occur in cells subjected to stress or damage. The types of programmed cell death are
indicated in black rectangles. The death of a cell (cell death, indicated in rectangles with dotted lines) can occur by "suicide"
(programmed cell death) or by "murder" (the cell death results from exposure to toxic compounds, severe stress caused by heat
or cold, or severe damage that causes irreversible immediate harm to the membrane or cellular organelles).

disparadas en circunstancias distintas (Guimares y Linden, andfemale flowers, usually the flowers are originally
2004; Wang et al., 2010; Nakaba et al., 2011; Wang y Zhang, bisexual and the development of male flowers involves the
2011) y por consiguiente existen diferencias en los cambios PCD of the stigma, style and ovary; and the formation of the
morfolgicos que sufren las clulas que mueren. Algunos feminine flower results from the death of the developed
ejemplos de MCP que comnmente se presentan en plantas stamens; 3) self-fertilization is prevented by PCD of the
se pueden mencionar: 1) la degeneracin de clulas stigma cells and/or the pollen tube; and 4) the formation of
especficas que ocurre durante el crecimiento del embrin y xylem by the death of vessels and cells that constitute
germinacin (las clulas suspensoras del embrin y las del tracheids, fibers and sclereids.
escutelum y endospermo mueren), la muerte de los The information that has been generated in studies
cotiledones, ptalos, carpelos y otras partes florales y de concerning PCD in metazoans, has provided the basis for
clulas parenquimatosas en la formacin del aernquima; 2) grouping the different types of PCD into three categories,
la diferenciacin de flores masculinas y femeninas, considering both morphological characteristics presented
usualmente las flores son originalmente bisexuales y el by cells that die, as well as the type of cellular organelle
desarrollo de flores masculinas involucra la MCP del involved in the death: 1) apoptosis; 2) lysosomal death
estigma, estilo y ovario; y la formacin de la flor femenina (autophagy); and 3) non-lysosomal death (Schweichel and
resulta de la muerte de los estmenes desarrollados; 3) la Merkel, 1973; Baehrecke, 2003; Williams and Dickman,
prevencin de autofecundacin por MCP de las clulas del 2008). In apoptosis, the cell destined to die is devoured by a
estigma y/o del tubo de polen; y 4) la formacin de xilema live cell (a kind of "cannibalism") whichis is degraded in its
por muerte de elementos de los vasos y de las clulas que se lysosome (cellular organelle in which hydrolytic enzymes
REVISTA MEXICANA DE FITOPATOLOGA/157

constituyen en traqueidas, fibras y esclereidas. that carry out intracellular or extracellular digestion of
La informacin que se ha generado en estudios macromolecules are stored); in autophagy or lysosomal cell
concerniente a la MCP en metazoarios, ha proporcionado las death the dying cell self-destructs using its own lysosomal
bases para agrupar en tres categoras a los diferentes tipos de system; and in the non-lysosomal death lysosomal
MCP, considerando tanto las caractersticas morfolgicas degradation is not involved and is a kind of less common
que presentan las clulas que fallecen, como el tipo de PCD (van Doorn and Woltering, 2005). Several studies
organelo celular involucrado en el fallecimiento: 1) indicate that most documented examples of PCD during
apoptosis; 2) muerte lisosomal (autofagia) y 3) muerte no plant development fall into the category of autophagic
lisosomal (Schweichel y Merkel, 1973; Baehrecke, 2003; death, having no examples to date of apoptosis or autophagy
Williams y Dickman, 2008). En la apoptosis, la clula (van Doorn and Woltering, 2005; 2008; Woltering et al.,
destinada a fallecer es devorada por una viva (es una especie 2010; Yoshimoto, 2010).
de canibalismo) que la degrada en su lisosoma (organelo Hypersensitivity response (HR). HR is defined as a
celular en el que almacenan enzimas hidrolticas que llevan rapid death of plant cells associated with the restriction of
a cabo la digestin intracelular o extracelular de pathogen growth (Mur et al., 2008; Vidhyasekaran, 2008)
macromolculas); en la autofagia o muerte celular lisosomal and is generally recognized by the presence of one or several
la clula que muere se autodestruye utilizando su propio dead cells with brown coloration at the infection site. The
sistema lisosomal; y en la muerte no lisosomal no est brown lesion can be seen at the macroscopic level when it
involucrada la degradacin lisosomal y es un tipo de MCP involves a sufficient number of cells, however, in some
menos frecuente (van Doorn y Woltering, 2005). En varias cases necrosis is only visible at a microscopic level when
investigaciones indican que la mayora de los ejemplos few cells are involved in the HR. It has been recorded that
documentados de MCP durante el desarrollo de la planta se plants in which HR, has been triggered show a certain degree
ubican en la categora de muerte autofgica, no teniendo a la of resistance to pathogens in tissues distant from the site
fecha ejemplos de muerte del tipo apopttico y algunos where the reaction occurred, this type of protection is known
casos no corresponden ni a apoptosis ni a autofagia (van as systemic acquired resistance (SAR) and salicylic acid
Doorn y Woltering, 2005; 2008; Woltering et al., 2010; (SA) is apparently essential for its induction (Vlot et al.,
Yoshimoto, 2010). 2008; Hammerschmidt, 2009).
Respuesta de hipersensibilidad (RH). La RH se It was initially considered that HR was a
define como una muerte rpida de clulas vegetales asociada characteristic response of resistant plants and that it only
con la restriccin del crecimiento de patgenos (Mur et al., went off in situations where there was a gene to gene
2008; Vidhyasekaran, 2008) y generalmente se reconoce por relationship. On the other hand, it was assumed that the
la presencia de una o varias clulas muertas con coloracin product of the avirulence gene avr, which acts as a race
caf en el sitio de infeccin. La lesin caf puede specific elicitor, interacted with the corresponding
visualizarse a nivel macroscpico cuando involucra a un resistance gene (R) product; that is, that it was only present
nmero suficiente de clulas; no obstante, en algunos casos in incompatible type interactions. However, we now know
la necrosis solamente es visible al microscpico cuando son that the HR is expressed both in host as well as in non-host
pocas las clulas involucradas en la RH. Se ha consignado plants and is controversial if the genetic control is the same
que las plantas en las que se dispara la RH, muestran cierto in both cases (Heath, 2000; Lenk and Thordal-Christensen,
grado de resistencia a patgenos en tejidos distantes al sitio 2009; Lipka et al., 2010). Studies with mutants of maize
donde ocurri la reaccin; este tipo de proteccin se le (Zea mays), tomato (Solanum lycopersicum) and
conoce como resistencia sistmica adquirida (RSA) y el Arabidopsis thaliana (L.) Heynh, have revealed that HR
cido saliclico (AS) es, al parecer esencial para su also depends on additional genes that appear to be present in
induccin (Vlot et al., 2008; Hammerschmidt, 2009). both resistant and susceptible individuals, and give the plant
Inicialmente se consider que la RH era una the ability to hypersensitively respond even in situations
respuesta caracterstica de plantas resistentes y que se where there is no R-avr relationship (Heath, 2000; Lipka et
disparaba solamente en aquellas situaciones en la que exista al., 2010). Furthermore, to date a few specific elicitors have
una relacin gen a gen. Por otro lado, se asuma que el been isolated and also several oomycete fungi produce a
producto del gen de avirulencia (avr), que acta como variety of metabolites, that form part of their component or
elicitor especfico de raza, interaccionaba con el producto secretions (carbohydrates from the cell wall, proteins and
del gen de resistencia (R) correspondiente; esto es, que glycoproteins), known as non-specific elicitors, which can
nicamente se presentaba en interacciones de tipo induce the plant's defense responses, and in some cases
incompatible. Sin embargo, en la actualidad se sabe que la cellular death (Heath, 2000; Mishra et al., 2009).
RH se expresa tanto en plantas hospedantes como en no Phytopathogenic bacteria such as Pseudomonas syringae,
hospedantes y es controversial si el control gentico es el Erwinia amylovora and Ralstonia solanacearum, amongst
mismo en ambos casos (Heath, 2000; Lenk y Thordal- others, have protein elicitors that trigger the HR (Grant and
Christensen, 2009; Lipka et al., 2010). Estudios con Mansfield, 1999; El-Maarouf et al., 2001; Gimenez-Ibanez
mutantes de maz (Zea mays), tomate (Solanum and Rathjen, 2010). The oomycetes Phytophthora
lycopersicum) y Arabidopsis thaliana (L.) Heynh, han cryptogea and P. capsici produce the proteins cryptogein
revelado que la RH tambin depende de genes adicionales and capsicein, respectively, which act as elicitors
que parecen estar presentes tanto en individuos resistentes (Nespoulous et al., 1999; Sawai et al., 2010).
158/VOLUMEN 29, NMERO 2, 2011

como susceptibles, y que le confieren a la planta la habilidad Even when it is considered that HR in plants is the maximum
de responder hipersensitivamente an en situaciones donde expression of resistance to pathogen attack, it is not always
no existe la relacin R-avr (Heath, 2000; Lipka et al., 2010). effective to protect them from the attack. Its efficiency to
Asimismo, a la fecha se han aislado pocos elicitores stop the advance of the pathogen is largely determined by its
especficos y tambin algunos hongos oomicetos producen dietary habit, if it is biotrophic, hemibiotrophic or
una variedad de metabolitos, que forman parte de sus necrotrophic and if it grows intra or extracellularly
componentes o secreciones (carbohidratos de la pared (Grenville-Briggs and van West, 2005; Kliebenstein and
celular, protenas y glicoprotenas), conocidos como Rowe, 2008; Mnch et al., 2008). The successful
elicitores no especficos, que pueden inducir las respuestas colonization of the host tissue by the pathogen will depend
de defensa de las plantas, y en algunos casos la muerte on whether it has the ability to draw on at least one of the
celular (Heath, 2000, Mishra et al., 2009). Bacterias following strategies: 1) have the ability to evade the
fitopatgenas como Pseudomonas syringae, Erwinia detection system (surveillance) of the plant by not producing
amylovora y Ralstonia solanacearum, entre otras, poseen elicitor molecules that could give it away, or if it does
elicitores protenicos que disparan la RH (Grant y produce them, "camouflage" them in a way that they are not
Mansfield, 1999; El-Maarouf et al., 2001; Gimenez-Ibanez detected by the host; 2) even when it produces elicitor
y Rathjen, 2010). Los oomicetos Phytophthora cryptogea y molecules, it can interfere with the defense responses, for
P. capsici producen las protenas criptogeina y capsiceina, example through detoxification of antimicrobial
respectivamente, que actan como elicitores (Nespoulous et compounds; 3) have a high rate of growth (or mobilization
al., 1999; Sawai et al., 2010). such as phytonematodes) so that it can get away quickly
An cuando se considera que la RH en plantas es la from the site where the highest defense response is taking
mxima expresin de resistencia al ataque por patgenos, place; 4) have a feeding habit that is as close to necrotrophic
esta no siempre resulta efectiva para protegerla del ataque as possible (organisms that kill cells to use as a food
de stos. Su eficacia para detener el avance del patgeno esta substrate), so that by killing an extensive area of host cells,
en gran medida determinada por el hbito alimenticio de through the production of large quantities of toxins or
ste, biotrfico, hemibiotrfico o necrotrfico y si crece enzymes, it will interfere with the active defense responses
intra o extracelularmente (Grenville-Briggs y van West, (production of phytoalexins and other antimicrobial
2005; Kliebenstein y Rowe, 2008; Mnch et al., 2008). La metabolites, cell wall thickening and callose accumulation,
colonizacin exitosa del tejido hospedante por el patgeno among others) that the neighboring living cells perform.
depende de si ste tiene la capacidad de ejercer por lo menos Currently, the evidences we have that show that HR
alguna de las siguientes estrategias: 1) tener la capacidad de is a result from PCD processes are: the activation of cellular
evadir el sistema de deteccin (vigilancia) de la planta no death in absence of pathogens by the mutation of certain
produciendo molculas elicitoras que lo puedan delatar, o si genes that are considered to be involved in the death
las produce camuflajearlas de forma que no sean pathway; the activation of the death when elicitors produced
detectadas por el hospedante; 2) an cuando produzca las by the pathogen are recognized; and the activation of the HR
molculas elicitoras, poder interferir con las respuestas de by transgenes in plants (Mittler and Rizhsky, 2000; Rostoks
defensa, por ejemplo mediante detoxificacin de et al., 2003; Lenk and Thordal-Christensen, 2009; Mishra et
compuestos antimicrobianos; 3) poseer una tasa alta de al., 2009; Sawai et al., 2010). The fact that a death similar to
crecimiento (o de movilizacin como los fitonematodos) de HR can be activated in the absence of the pathogen suggests
modo que pueda alejarse rpidamente del sitio en el que se that this type of cellular death is not directly caused by the
estn dando con mayor intensidad las respuesta de defensa; invading pathogen, but rather results from the activation of a
4) tener un hbito alimenticio que se acerque ms al extremo specific PCD pathway in the host (Lakimova et al., 2005).
de los necrotrficos (organismos que asesinan a las clulas Several studies indicate that the existence of mutants, that
para utilizarlo como substrato alimenticio), de manera que al spontaneously activate the HR in absence of a pathogen, is
asesinar un rea extensiva de clulas hospedantes, mediante the strongest evidence that the HR is a PCD process. These
la produccin de grandes cantidades de toxinas o enzimas, mutants known as "disease lesion mimics" and mutations
interfiera con las respuestas de defensa activa (produccin that cause HR lesions in the absence of pathogens probably
de fitoalexinas y otros metabolitos antimicrobianos, occur in genes that control PCD; for this, such mutants
engrosamiento de paredes celulares y acumulacin de constitute a powerful tool in the study of HR in plants
calosa, entre otras) que llevan a cabo las clulas vivas (Rostoks et al., 2003; Lakimova et al., 2005; Love et al.,
vecinas. 2008; Lenk and Thordal-Christensen, 2009).
En la actualidad las evidencias que se tienen de que la Morphological and structural changes that occur
RH resulta de procesos de MCP son: la activacin del in the HR. The morphological and structural changes
fallecimiento celular en ausencia de patgenos por mutacin accompanying the PCD during the plant-microorganism
de ciertos genes que se considera estn involucrados en la interactions have been studied in a few plant-pathogen
ruta de muerte; la activacin de la muerte cuando elicitores interactions. In those models that have been studied, the
producidos por el patgeno son reconocidos; y la activacin stopping of the cytoplasmic stream followed by the
de la RH por transgenes en plantas (Mittler y Rizhsky, 2000; dismantling of the protoplast and the fragmentation of the
Rostoks et al., 2003; Lenk y Thordal-Christensen, 2009; nuclear deoxyribonucleic acid (DNA) are early events that
Mishra et al., 2009; Sawai et al., 2010). El hecho de que una take place consistently during the HR.
REVISTA MEXICANA DE FITOPATOLOGA/159

muerte similar a la RH pueda activarse en la ausencia del In soybean (Glycine max) cells in suspension and inoculated
patgeno, sugiere que este tipo de fallecimiento celular no es with an avirulent strain of P. syringae pv. glycinea a PCD
directamente causado por el patgeno invasor sino que was observed; accompanied by DNA fragmentation,
resulta de la activacin de una ruta especfica determinada blebbing of the plasma membrane, condensation of the
de MCP en el hospedante (Lakimova et al., 2005). En varias nucleus and cytoplasm, and cell shrinkage (Levine et al.,
investigaciones se indica que la existencia de mutantes que 1996). When the inoculation of the bacteria took place in full
espontneamente activan la RH en ausencia de un patgeno, leaves, these authors observed that the internal structure of
constituye la evidencia ms contundente de que la RH es un the chloroplast was lost and starch grains had accumulated
proceso de MCP. Estos mutantes conocidos como mutantes in the stroma, and mesophyll cells showed shrinkage and
que imitan lesiones de enfermedad (disease lesion fragmentation of the protoplast. Such changes were not
mimics) y las mutaciones que causan la aparicin de observed in the interaction compatible with the virulent
lesiones de RH en la ausencia de patgenos probablemente strain, which did not cause a HR. Also, cells in tobacco
ocurren en genes que controlan la MCP; por lo anterior, tales (Nicotiana tabacum), not hosting the oomycete P.
mutantes constituyen una herramienta poderosa para el cryptogea, treated with cryptogein suffered morphological
estudio de la RH en plantas (Rostoks et al., 2003; Lakimova changes similar to those observed in soybean cells with the
et al., 2005; Love et al., 2008; Lenk y Thordal-Christensen, avirulent strain of P. syringae pv. glycinea. In a cultivar of
2009). pumpkin (Cucurbita maxima) resistant to P. capsici the
Cambios morfolgicos y estructurales que parenchymal cells of the infected stem suffered plasmolysis
ocurren en la RH. Los cambios morfolgicos y of the plasma membrane and the cytoplasmic material, and
estructurales que acompaan a la MCP durante las the nucleus were attached in the contact site of the hyphae of
interacciones planta-microorganismo han sido investigados the oomycete. On the other hand, in the susceptible cultivar
en pocas interacciones planta-patgeno. En aquellos the plasma membrane of infected cells was disorganized, the
modelos que se han estudiado, el detenimiento de la cells plasmolyzed and their chloroplasts were deformed and
corriente citoplasmtica seguido por el desmantelamiento showed disorganization in their membrane system (Lee et
del protoplasto y la fragmentacin del cido al., 2001). Similar morphological and structural changes
desoxirribonucleico (ADN) nuclear son eventos tempranos have also been reported in fruits that have a hypersensitive
que se presentan consistentemente durante la RH. response; the fruit of chile (Capsicum baccatum) resistant to
En clulas de soya (Glycine max) en suspensin e Colletotrichum gloeosporioides (Glomerella cingulata),
inoculadas con una cepa avirulenta de P. syringae pv. showed several cytological characteristics typical of PCD
glycinea se observ una MCP; acompaada de such as separation of the plasma membrane from the cellular
fragmentacin del ADN, globulacin de la membrana wall, cytoplasm condensation, dilation of endoplasmic
plasmtica, condensacin del ncleo y citoplasma, y reticulum, the presence of numerous small vacuoles,
contraccin de la clula (Levine et al., 1996). Cuando la heterochromatic and less osmophilic nucleus, and DNA
bacteria se inocul se hizo en hojas completas, estos fragmentation. In contrast, in susceptible fruit (C. annuum)
mismos autores observaron que la estructura interna del degradation of the cell wall, vacuole fragmentation,
cloroplasto se perdi y se acumularon granos de almidn en degradation of the cytoplasm and nucleus, and condensation
el estroma, y las clulas del mesfilo mostraron contraccin of the cytoplasm was observed (Kim et al., 2004). Several
y fragmentacin del protoplasto. Tales cambios no fueron researchers have proposed that in compatible interactions,
observados en la interaccin compatible con la cepa the death of host cells could also eventually be a PCD and
virulenta, la cual no provoc una RH. Clulas de tabaco involve similar mechanisms. However, it is convenient to
(Nicotiana tabacum), no hospedante del oomiceto P. comment that the structural changes that the researchers
cryptogea, tratadas con criptogeina tambin sufrieron observed in the compatible interactions in pumpkin-P.
cambios morfolgicos similares a los observado en clulas capsici and C. annuum-C. gloeosporioides, such as the
de soya con la cepa avirulenta de P. syringae pv. glycinea. En disorganization of the cell membrane, plasmolization of the
un cultivar de calabacita (Cucurbita maxima) resistente a P. cytoplasm, deformation of the chloroplasts and
capsici las clulas del parnquima del tallo infectado disorganization of the membrane system in the first case and
sufrieron plasmolisis de su membrana plasmtica, y el the degradation of the cell walls in susceptible fruit in the
material citoplsmico y el ncleo se agregaron en el sitio de second; these clearly show that the mechanisms that lead to
contacto de la hifa del oomiceto. Por otro lado, en el cultivar the death of the cells were totally different from those that
susceptible la membrana plasmtica de las clulas occurred in the HR, and that the host cells were killed by the
infectadas fue desorganizada, las clulas se plasmolizaron y pathogen, by the introduction of toxins and/or enzymes that
sus cloroplastos se deformaron y mostraron degrade the cell walls and structural compounds of the cell
desorganizacin en su sistema de membranas (Lee et al., membranes and whose direct harmful effects on the
2001). Cambios morfolgicos y estructurales similares han structural components or the host cell's metabolic pathways
sido reportados tambin en frutos respondiendo have been widely documented (Hckelhoven, 2007;
hipersensitivamente; as frutos de chile (Capsicum Eichmann and Hckelhoven, 2008; Ribot et al., 2008).
baccatum) resistentes a Colletotrichum gloeosporioides The DNA fragmentation in oligonucleotides of
(Glomerella cingulata), mostraron varias caractersticas different sizes, has been observed during the HR in several
citolgica tpicas de la MCP como separacin de la plant-pathogen interactions; for example, in tobacco leaf
160/VOLUMEN 29, NMERO 2, 2011

membrana plasmtica de la pared celular, condensacin del cells with the N gene (which gives resistance against the
citoplasma, dilatacin del retculo endoplasmico, presencia tobacco mosaic virus=TMV) and infected with TMV DNA
de numerosas vacuolas pequeas, ncleo heterocromtico y fragments of approximately 50,000 base pairs (bp) were
menos osmofilico, y fragmentacin del ADN. En contraste, observed; likewise, Levine et al. (1996) observed that in the
en frutos susceptibles (C. annuum) se observ degradacin PCD developed in the incompatible interaction soybean-P.
de la pared celular, fragmentacin de vacuolas, degradacin syringae pv. glycinea, the DNA was broken into similar
del ncleo y citoplasma, y condensacin del citoplasma sized fragments. On the other hand, the HR in cowpea
(Kim et al., 2004). Algunos investigadores han propuesto (Vigna unguiculata) inoculated with Uromyces vignae
que en interacciones compatibles, la muerte de clulas (Ryerson and Heath, 1996; Heath et al., 1997), and in the oat
hospedantes podra tambin finalmente constituir una MCP (Avena sativa)-Puccinia coronata and A. thaliana-P.
e involucrar mecanismos similares. Sin embargo, es syringae interactions, the division of the nuclear DNA
conveniente comentar que los cambios estructurales que los generated small fragments consistent in multiples of 180 bp
investigadores observaron en las interacciones compatibles (Greenberg and Yao, 2004).
calabacita-P. capsici y C. annuum-C. gloeosporioides, tales The caspases are the executor molecules of the PCD
como la desorganizacin de las membrana plasmtica, in animals (Khurana et al., 2005; Fernando and Megeney,
plasmolizacin del citoplasma, deformacin de los 2007; Chowdhury et al., 2008; Woltering, 2010). These
cloroplastos y desorganizacin de su sistema de membranas proteinases possess an active cysteine-based site and
en el primer caso, y la degradacin de paredes celulares en separate the aspartic acid residues breaking the bond that
los frutos susceptibles en el segundo; son situaciones que keeps it joined the polypeptide substrate together
claramente evidencian que los mecanismos que condujeron (Hengartner, 2000; Sanmartin et al., 2005; Woltering,
al fallecimiento de las clulas fueron totalmente diferentes 2010). The results from molecular and biochemical, studies
de aquellos que ocurrieron en la RH, y que las clulas support the hypothesis that enzymes similar to the caspases
hospedantes fueron asesinadas por el patgeno por la are involved in the HR in plants (Coll et al., 2010), as the HR
produccin de toxinas y/o enzimas que degradan paredes was suppressed when synthetic peptide inhibitors of the
celulares y compuestos estructurales de las membranas caspases were applied (del Pozo and Lam, 2003) and even
celulares y cuyos efectos nocivos directos sobre though, for now, caspase enzymes have not been identified
componentes estructurales o rutas metablicas de las clulas in plants, there exists information that suggests the existence
hospedantes ha sido ampliamente documentados of proteases that have an active cysteine-based site. This
(Hckelhoven, 2007; Eichmann y Hckelhoven, 2008; supports the idea that there are proteases with caspase,
Ribot et al., 2008). activity in plants that participate in the PCD. It has also been
La fragmentacin del ADN en oligonucletidos de suggested that small proteins of the Ras, family belonging to
diferentes tamaos, se ha observado durante la RH en varias the G, superfamily (small proteins that bind to
interacciones planta-patgeno; por ejemplo, en clulas de GDP=guanosine diphosphate) and that also function as PCD
hojas de tabaco con el gen N (que confiere resistencia al executing molecules in animals, they could also be involved
virus mosaico del tabaco=VMT) e infectadas con VMT se in PCD in plants. The Ras proteins are important in the
observaron fragmentos de ADN de aproximadamente plant's, cellular cycle by binding to GDP and to cysteine
50,000 pares de bases (pb); asimismo, Levine et al. (1996) sensitive proteases Lakimova et al., 2005; Srmo et al.,
observaron que en la MCP que se present en una 2006).
interaccin incompatible soya-P. syringae pv. glycinea el Cascade of biochemical events that occur in the
ADN se rompi en fragmentos de tamao similar. Por otro HR. Once the interaction of the effector (E) molecule
lado, la RH en hojas de frijol caup (Vigna unguiculata) (produced by the pathogen) with the receptor (R) molecule
inoculadas con Uromyces vignae (Ryerson y Heath, 1996; occurs in the surface or inside of the plant cell, it triggers a
Heath et al., 1997), y en las interacciones avena (Avena cascade of events that include the activation of multiple
sativa)-Puccinia coronata y A. thaliana-P. syringae, la signal transduction pathways into the invaded cell and
divisin del ADN nuclear gener fragmentos pequeos involve the oxidative burst through which oxygen-reactive
-
consistentes en mltiplos de 180 pb (Greenberg y Yao, species are produced (H2O2, hydrogen peroxide; O2 ,
-
2004). superoxide anion; and OH , hydroxyl radical); the flow of
+ + 2+
Las caspasas son las molculas ejecutoras de la MCP ions such as H , K and Ca ; the activity of kinases and
en animales (Khurana et al., 2005, Fernando y Megeney, phosphatases that transmit and amplify the signal, whose
2007; Chowdhury et al., 2008; Woltering, 2010). Estas ultimate target are usually the transcription factors that
proteinasas poseen un sitio activo a base de cistena y regulate gene expression. The expressed genes are those that
separan a los residuos de cido asprtico rompiendo el encode for peroxidases and enzymes key to the secondary
enlace que lo mantiene unido al substrato polipeptdico metabolism pathways (such as PAL=phenylalanine
(Hengartner, 2000; Sanmartn et al., 2005; Woltering, ammonia-lyase and HMG-CoAr=3-hydroxy-3-
2010). Los resultados de estudios moleculares y methylglutaryl-coenzyme A reductase) through which
bioqumicos, apoyan la hiptesis de que enzimas similares a compounds with antimicrobial properties are synthesized
las caspasas estn involucradas en la RH de las plantas (Coll (phenols and phytoalexins, for example); pathogenesis-
et al., 2010), pues la RH fue suprimida cuando se aplicaron related proteins (such as -glucanases and chitinases);
pptidos sintticos inhibidores de las caspasas (del Pozo y compounds (phenols and lignin) and proteins that reinforce
REVISTA MEXICANA DE FITOPATOLOGA/161

Lam, 2003) y aunque a la fecha no se han identificado and protect the cell walls against enzyme activity that
enzimas caspasas en plantas, existe informacin que sugiere degrade cell walls or interfere with the activity of these last
la existencia de proteasas que poseen un sitio activo a base mentioned such as polygalacturonase-inhibiting proteins
de cistena. Lo anterior sustenta la idea de que en plantas and hydroxyproline-rich glycoproteins (Soylu, 2006;
existen proteasas con actividad de caspasas, que participan Cvikrova et al., 2006; Menden et al., 2007; Godinez-Vidal et
en la MCP. Asimismo, se ha sugerido que protenas al., 2008; Sels et al., 2008; Schacht et al., 2011). Among the
pequeas de la familia Ras, pertenecientes a la superfamilia signals that are generated and that "sound the alarm", both at
G (protenas pequeas que se unen a GTP= trifosfato de a local level in neighboring cells and systemically are
guanosina) y que funcionan tambin como molculas ethylene and salicylic and jasmonic acids (Figure 2). These
ejecutoras de MCP en animales, podran igualmente estar defense responses are actually present in both compatible
involucradas en la MCP en plantas. Las protenas Ras son and incompatible interactions, and the difference lies in the
importantes en el ciclo celular de las plantas, al unirse a GTP speed and magnitude with which it is expressed in each
y a proteasas sensitivas a cistena (Lakimova et al., 2005; interaction.
Srmo et al., 2006).
A Cascada de eventos bioqumicos que ocurren en CONCLUSIONS
la RH. Una vez que ocurre la interaccin de la molcula The emphasis on HR, investigations has been on
efectora (E, producida por el patgeno) con la molcula biochemical and molecular changes that occur in the cells
receptora (R) en la superficie o interior de la clula vegetal, involved. The morphological and ultrastructural changes
se desata una cascada de eventos que incluyen la activacin that arise in hypersensitive, cells have been studied in
de mltiples rutas de transduccin de seales hacia el relatively few plant-pathogen models, as they simply
interior de la clula invadida y que involucran la explosin describe the colonization and morphological characteristics
oxidativa a travs de la cual se producen especies reactivas of the pathogen, and rarely do they include the
-
de oxgeno (H2O2, perxido de hidrgeno; O2 , anin ultrastructural changes that the organelles in host cells
-
superxido; y OH , radical hidroxilo); flujo de iones como suffer; however, by the structural and morphological
H+, K+ y Ca2+; la actividad de cinasas y fosfatasas que characteristics that the suicide cells show in the few models
transmiten y amplifican la seal, cuyo blanco ltimo that have been studied, it is considered that the HR is a PCD
Bgeneralmente son los factores de transcripcin que regulan of the lysosomal or autophagic type. On the other hand, to
la expresin de genes. Los genes expresados son aquellos this day, the existence of caspase proteins has not been
que codifican para peroxidasas y enzimas clave de las rutas demonstrated in plants, these proteins, which have been
del metabolismo secundario (como PAL=fenilalanina signaled as the executor molecules of PCD in animals. The
amonio liasa y HMG-CoAr=3-hidroxi-3-metilglutaril molecular and biochemical studies currently available on
coenzima A reductasa), a travs de las cuales se sintetizan plants support the hypothesis that enzymes with similar
compuestos con propiedades antimicrobianas (fenoles y functions to those of the caspases are involved in the
fitoalexinas, por ejemplo); protenas relacionadas con execution of the hypersensitive cells, hence it is of
patognesis (como -glucanasas y quitinasas); compuestos fundamental importance to identify the enzymes involved in
(fenoles y lignina) y protenas que refuerzan y protegen a las PCD's in plants and determine their similarity to caspases in
paredes celulares contra la actividad de enzimas que animals. Future research on the HR should consider a larger
degradan paredes celulares, o que interfieren con la number of plant-pathogen interaction models including
actividad de stas ltimas, como las protenas inhibidoras de those in which there is no clear gene to gene relationship.
poligalacturonasas y glicoprotenas ricas en hidroxiprolina Also, in addition to comparing and contrasting the
(Soylu, 2006; Cvikrov et al., 2006; Menden et al., 2007; morphological and structural changes that occur in
Godinez-Vidal et al., 2008; Sels et al., 2008; Schacht et al., compatible (pathogenesis-induced necrosis) and
2011). Entre las seales que se generan y que alertan, tanto incompatible interactions (HR-induced necrosis), we must
a nivel local en las clulas vecinas, como de manera deepen the understanding of the fine biochemical
sistmica son el etileno y los cidos saliclico y jasmnico mechanisms that lead to cell death, to thereby have sufficient
(Figura 2). Todas estas respuestas de defensa en realidad se experimental evidence to determine whether there are
presentan tanto en interacciones compatibles como en significant differences at this level when the cell commits
incompatibles y la diferencia radica en la rapidez y la suicide (HR) with the "intention" of defending itself from
magnitud con la que se expresan en cada interaccin. attack by the pathogen and when it is killed by it.

CONCLUSIONES LITERATURA CITADA


El nfasis en las investigaciones de la RH, se ha Ameisen JC. 2002. On the origin, evolution, and nature of
puesto en los cambios bioqumicos y moleculares que programmed cell death: a timeline of four billion years.
ocurren en las clulas involucradas. Los cambios Cell Death and Differentiation 9:367-393.
morfolgicos y ultraestructurales que se presentan en las Baehrecke EH. 2003. Autophagic programmed cell death in
clulas hipersensitivas, se han estudiado en relativamente Drosophila. Cell Death and Differentiation 10:940-945.
pocos modelos planta-patgeno, pues se limitan a describir Chowdhury I, Tharakan B and Bhat GK. 2008. Caspases-an
la colonizacin y caractersticas morfolgicas del patgeno, update. Comparative biochemistry and physiology Part
y pocas veces se incluyen los cambios ultraestructurales que B. Biochemistry and Molecular Biology 151:10-27.
162/VOLUMEN 29, NMERO 2, 2011

Flujo de iones: Generacin extracelular


R 2+ + + de especies reactivas de
Ca , H , K
O2

MC
E
C
R Involucramiento de la
actina de citoesqueleto
L
U ?
L
Fosforilacin de protenas
A

H Sntesis de protenas

O CITOPLASMA
S
cido saliclico
P
E
D Generacin de seales y Liberacin de elicitores
MUERTE CELULAR
A movilizacin a distancia endgenos

N
T
E
INDUCCIN DE RESISTENCIA INDUCCIN DE RESPUESTAS
SISTMICA ADQUIRIDA EN LA DE DEFENSA EN CLULAS
PLANTA COMPLETA ADYACENTES
(Alteraciones en las rutas de metabolismo secundario, (Alteraciones en las rutas de metabolismo secundario,
produccin de etileno y cido jasmnico, sntesis de PRP, produccin de etileno y cido
sntesis de peroxidasas, glucanasas jasmnico, fortificacin de paredes
y otras PRP) celulares: lignina, PGIPs, HRGPs)

Figura 2. Secuencia de eventos que ocurren en la muerte celular hipersensitiva en algunas interacciones planta-patgeno.
E=Elicitor producido por el patgeno y que puede ser especfico (producto de un gen de avirulencia, avr) o no especfico.
R=Receptor producto o no de un gen de resistencia (R) del hospedante y que puede estar presente en la membrana celular (MC)
o en el citoplasma. PRP=Protenas relacionadas con patognesis. PGIPs=Protenas inhibidoras de poligalacturonasas.
HRGPs=Glucoprotenas ricas en hidroxiprolina.
Figure 2. Sequence of events that take place in the hypersensitive cell death in some plant-pathogen interactions. E=Elicitor
produced by the pathogen and may be specific (product of an avirulence gene, avr) or nonspecific. R=Receptor product or not
from a resistance gene (R) of the host and that may be present in the cell membrane (CM) or in the cytoplasm.
PRP=Pathogenesis-related proteins. PGIPs=Polygalacturonase Inhibiting proteins. HRGPs=Hydroxyproline-rich
glycoproteins.
sufren los organelos de las clulas hospedantes; no obstante, Camarena GG. 2006. Muerte celular programada como
por las caractersticas estructurales y morfolgicas que respuesta al estrs ambiental. Revista Chapingo. Serie
muestran las clulas suicidas, en los pocos modelos en los Ciencias Forestales y del Ambiente 12:93-99.
que se han estudiado, se considera que la RH es una MCP del Coll NS, Vercammen D, Smidler A, Clover C, Breusegem
tipo lisosomal o autofgica. Por otro lado, a la fecha no se ha F, van Dangl JL and Epple P. 2010. Arabidopsis type I
demostrado la existencia de protenas caspasas en plantas, metacaspases control cell death. Sciences 330:1393-
mismas que en animales se han sealado como las molculas 1397.
ejecutoras de la MCP. Los estudios moleculares y Cvikrova M, Mala J, Hrubcova M and Eder J. 2006. Soluble
bioqumicos por ahora disponibles en plantas, apoyan la and cell wall-bound phenolics and lignin in Ascocalyx
hiptesis de que enzimas con similitud funcional a las abietina infected Norway spruces. Plant Science
caspasas, estn involucradas en la ejecucin de las clulas 170:563-570.
hipersensitivas, de ah que es de fundamental importancia Del Pozo O and Lam E. 2003. Expression of the
identificar las enzimas involucradas en la MCP en plantas y baculovirusp35 protein in tobacco affects cell death
determinar su semejanza con las caspasas de animales. progression and compromises N-gene mediated disease
REVISTA MEXICANA DE FITOPATOLOGA/163

Futuras investigaciones acerca de la RH debern considerar invasion hyphae of the cowpea rust fungus. New
un mayor nmero de modelos de interaccin planta- Phytologist 135:689-700.
patgeno incluyendo aquellas en las que no existe una clara Hengartner MO. 2000. The biochemistry of apoptosis.
relacin gen a gen. Tambin, adems de comparar y Nature 407:770-776.
contrastar los cambios morfolgicos y estructurales que se Hckelhoven R. 2007. Cell wall-associated mechanisms of
dan en las interacciones compatibles (necrosis por disease resistance and susceptibility. Annual Review of
patognesis) e incompatibles (necrosis por RH), habr que Phytopathology 45:101-129.
profundizar en el entendimiento de los mecanismos Jimenez C, Capasso JM, Edelstein CL, Rivard CJ, Lucia S,
bioqumicos finos que conducen a la muerte celular, para de Breusegem S, Berl T and Segovia M. 2009. Different
esta manera contar con la suficiente evidencia experimental ways to die: cell death modes of the unicellular
que permita determinar si existen o no diferencias chlorophyte Dunaliella viridis exposed to various
importantes a este nivel cuando la clula se suicida (RH) con environmental stresses are mediated by the caspase-like
la intencin de defenderse del ataque por el patgeno y activity DEVDase. Journal of Experimental Botany
cuando es asesinada por ste. 60:815-828.
Kaczanowski S, Sajid M and Reece SE. 2011. Evolution of
resistance response to tobacco mosaic virus. Molecular apoptosis-like programmed cell death in unicellular
Plant-Microbe Interactions 16:485-494. protozoan parasites. Parasites and Vectors 4:44.
Eichmann R and Hckelhoven R. 2008. Accommodation of K h u r a n a S M P, P a n d e y S K , S a r k a r D A a n d
powdery mildew fungi in intact plant cell. Journal of Chanemougasoundharam A. 2005. Apoptosis in plant
Plant Physiology 165:5-18. disease response: a close encounter of the pathogen kind.
El-Maarouf H, Barny MA, Rona JP and Bouteau F. 2001. Current Science 88:740-752.
Harpin, a hypersensitive response elicitor from Erwinia Kim KH, Yoon JB, Park HG, Park EW and Kim YH. 2004.
amylovora, regulates ion channel activities in Structural modifications and programmed cell death of
Arabidopsis thaliana suspension cells. FEBS Letters chili pepper fruit related to resistance responses to
497:82-84. Colletotrichum gloeosporioides infection.
Fernando P and Megeney L. 2007. Is caspase-dependent Phytopathology 94:1295-1304.
apoptosis only cell differentiation take to the extreme? Kliebenstein DJ and Rowe HC. 2008. Ecological cost of
The FASEB Journal 21:8-17. biotrophic versus necrotrophic pathogen resistance, the
Gimenez-Ibanez S and Rathjen JP. 2010. The case for the hypersensitive response and signal transduction. Plant
defense: plant versus Pseudomonas syringae. Microbes Sciences 174:551-556.
and Infection 12:428-437. Lakimova ET, Michalczuk L and Woltering EJ. 2005.
Godnez-Vidal D, Rocha-Sosa M, Sepulveda-Garca EB, Hypersensitive cell death in plants-its mechanisms and
Lara-Reyna J, Rojas-Martnez R and Zavaleta-Meja E. role in plant defense against pathogens. Journal of Fruit
2008. Phenylalanine ammonia lyase activity in chilli and Ornamental Plant Research 13:135-158.
CM-334 infected by Phytophthora capsici and Nacobbus Lee BK, Hong JK and Hwang BK. 2001. Ultraestructure of
aberrans. European Journal of Plant Pathology 120:299- compatible and incompatible interactions of pumpkin
303. stems infected with Phytophthora capsici. The Plant
Grant M and Mansfield J. 1999. Early events in host- Pathology Journal 17:29-35.
pathogen interactions. Current Opinion in Plant Biology Lenk A and Thordal-Christensen H. 2009. Nonhost
2:312-319. resistance to lesion-mimic mutants: useful for studies of
Greenberg JT. 1997. Programmed cell death in plant- defense signaling. Advances in Botanical Research
pathogen interactions. Annual Review of Plant 51:91-121.
Physiology and Plant Molecular Biology 48:525-545. Levine A, Pennell RI, Alvarez ME, Palmer R and Lamb C.
Greenberg JT and Yao N. 2004. The role and regulation of 1996. Calcium-mediated apoptosis in a plant
programmed cell death in plant-pathogen interactions. hypersensitive disease resistance response. Current
Cellular Microbiology 6:201-211. Biology 6:427-437.
Grenville-Briggs LJ and van West P. 2005. The biotrophic Lipka U, Fuchs R, Kuhns C, Petutschnig E and Lipka V.
stages of oomycete-plant interactions. Advances in 2010. Live and let die-Arabidopsis nonhost resistance to
Applied Microbiology 57:217-243. powdery mildews. European Journal of Cell Biology
Guimares CA and Linden R. 2004. Programmed cell death. 89:194-999.
Apoptosis and alternative deathstyles. European Journal Love AJ, Milner JJ and Sadanandom A. 2008. Timing is
of Biochemistry 271:1638-1650. everything: regulatory overlap in plant cell death. Trends
Hammerschmidt R. 2009. Systemic acquired resistance. in Plant Science 13:589-595.
Advances in Botanical Research 51:173-222. Menden B, Kohlhoff M and Moerschbacher BM. 2007.
Heath MC. 2000. Hypersensitive response-related death. Wheat cells accumulate a syringyl-rich lignin during the
Plant Molecular Biology 44:321-334. hypersensitive resistance response. Phytochemistry
Heath MC, Nimchuk ZL and Xu H. 1997. Plant nuclear 68:513-520.
migrations as indicators of critical interactions between Mishra AK, Sharma K and Misra RS. 2009. Purification and
resistant or susceptible cowpea epidermal cells and characterization of elicitor protein from Phytophthora
164/VOLUMEN 29, NMERO 2, 2011

calocasiae and basic resistance in Colocasia esculenta. activity in tomato stem extracts. Plant Physiology and
Microbiological Research 164:688-693. Biochemistry 49:377-387.
Mittler R and Rizhsky L. 2000. Transgene-induced lesion Schweichel JU and Merkel HJ. 1973. The morphology of
mimic. Plant Molecular Biology 44:335-344. various types of cell death in prenatal tissue. Teratology
Mnch S, Lingner U, Floss DS, Ludwig N, Sauer N and 7:253266.
Deising HB. 2008. The hemibiotrophic life style of Sels J, Mathys J, De Coninck BMA, Cammue BPA and De
Colletotrichum species. Journal of Plant Physiology Bolle MFC. 2008. Plant pathogenesis-related (PR)
165:41-51. proteins: a focus on PR peptides. Plant Physiology and
Mur LAJ, Kenton P, Lloyd AJ, Ougham H and Prats E. 2008. Biochemistry 46:941-950.
The hypersensitive response; the centenary is upon us but Soylu S. 2006. Accumulation of cell-wall bound phenolic
how much do we know? Journal of Experimental Botany compounds and phytoalexin in Arabidopsis thaliana
59:501- 520. leaves following inoculation with pathovars of
Nakaba S, Kubo T and Funada R. 2011. Nuclear DNA Pseudomonas syringae. Plant Science 170:942-952.
fragmentation during cell death of short-lived ray Srmo CG, Leiros I, Brembu T, Winge P, Os V and Bones
tracheids in the conifer Pinus densiflora. Journal of Plant AM. 2006. The crystal structure of Arabidopsis thaliana
Research 124:379-384. RAC7/ROP9: the first RAS superfamily GPTase from
Nespoulous N, Gaudemer O, Huet J and Pernollet J. 1999. the plant kingdom. Phytochemistry 67:2332-2340.
Characterization of elicitin-like phospholipases isolated van Doorn WG and Woltering EJ. 2005. Many ways to exit?
from Phytophthora capsici culture filtrate. FEBS Letters Cell death categories in plants. Trends in Plant Science
452:400-406. 10:117-122.
Reape TJ, Molony EM and McCabe PF. 2008. Programmed van Doorn WG and Woltering EJ. 2008. Physiology and
cell death in plant: distinguishing between different molecular biology of petal senescence. Journal of
modes. Journal of Experimental Botany 59:435-444. Experimental Botany 59:453-480.
Reape TJ and McCabe PF. 2010. Apoptotic-like regulation Vidhyasekaran P. 2008. Fungal pathogenesis in plants and
of programmed cell death in plants. Apoptosis 15:249- crops. Molecular biology and host defense mechanisms.
256. Second Edition. CRC Press. Florida, USA. 509p.
Ribot C, Hirsch J, Balzergue S, Tharreau D, Notteghem J, Vlot AC, Klessing DF and Park S. 2008. Systemic acquired
Lebrun M and Morel J. 2008. Susceptibility of rice to the resistance the elusive signal(s). Current Opinion in Plant
blast fungus, Magnoporthe grisea. Journal of Plant Biology 11:436-442.
Physiology 165:114-124. Wang C and Zhang S. 2011. A cascade signal pathway
Rostoks N, Schmierer D, Kudrna D and Kleinhofs A. 2003. occurs in self-incompatibility of Pyrus pyrifolia. Plant
Barley putative hypersensitive induced reaction genes: Signaling and Behavior 6:420-421.
genetic mapping, sequence analyses and differential Wang J, Li X, Liu Y and Zhao X. 2010. Salt stress induces
expression in disease lesion mimic mutants. Theoretical programmed cell death in Thellungiella halophila
and Applied Genetics 107:1094-1101. suspension-cultured cells. Journal of Plant Physiology
Ryerson DE and Heath MC. 1996. Cleavage of nuclear DNA 167:1145-1151.
into oligonucleosomal fragments during cell death Williams B and Dickman M. 2008. Plant programmed cell
induced by fungal infection or by abiotic treatments. The death: can't live with it; can't live without it. Molecular
Plant Cell 8:393-402. Plant Pathology 9:531-544.
Sanmartin M, Jaroszewski L, Raikhel NV and Rojo E. 2005. Woltering EJ. 2010. Death proteases: alive and kicking.
Caspases. Regulating death since the origin of life. Plant Trends in Plant Science 15:185-188.
Physiology 137:841-847. Woltering EJ, Iakimova ET, Erkan M and Aksoy U. 2010.
Sawai Y, Tamotsu S, Kuchits K and Sakai A. 2010. Effects of Programmed cell death and postharvest deterioration of
growth phase and cell density on cryptogein-induced horticultural produce. Acta Horticulturae 877:991-997.
programmed cell death in suspension-cultured tobacco Yoshimoto K. 2010. Physiological roles of autophagy in
BY-2 cells: development of a model system for 100% plants: does plant autophagy have a pro-death function?
efficient hypersensitive cell death. Cytologia 75:389- Plant Signaling and Behavior 5:494-496.
396. Zandbergen G, van Lder CGK, Heussler V and Duszenko
Schacht T, Unger C, Pich A and Wydra K. 2011. Endo-and M. 2010. Programmed cell death in unicellular parasites:
exopolygalacturonases of Ralstonia solanacearum are a prerequisite for sustained infection? Trends in
inhibited by polygalacturonase-inhibiting protein (PGIP) Parasitology 26:477-483.