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Plants can get cancer
Plum Phwiol.
Biochrm..
1998.
36 (3),
203-204
Letter to the Editor Plants can get cancer Thomas
Gaspar
lnstitut de Botanique B 22, UniversitC de Libge, Sart Tilman, B-4000 Libge. Belgique (Tel./Fax 32-4-366 38 59) (Received July 15, 1997: accepted September 29, 1997)
Abstract - This is a reply to a paper entitled “Why don’t plants get cancer”, with an opposite opinion, and with arguments. Although there are many similitudes betwen animal and plant cancerous cells and organisms, because plant cancerous cells cannot become circulating metastases, plant cancer at the end of a neoplastic progression has needed a specific definition. The typical plant cancer trait is the irreversible loss of organogenic totipotency, i.e. the capacity of cancerous cells to reorganize primary organogenic meristems. 0 Elsevier, Paris. Plant cancer / organogenic
totipotency
I reply to a paper entitled “Why don’t plants get cancer?‘, published by Doonan and Hunt [I], because I am convinced of the contrary. Is the divergence a simple question of concept? I have been working for fifteen years on the processesof habituation (loss of requirement of exogenous growth regulators for sustained growth in vitro) and vitrification (hyperhydric malformations) of in vitro cultured cells and shoots respectively. I came to the conclusion that both phenomena were taking part in neoplastic progressions (in the absence of pathogens), leading to true cancer cells (in calli) or to true generalized cancers at the organismic (shoot) level, with (programmed?) death as ultimate issues. I summarize herewith the arguments developed for such plant cancer concepts which where pre-reviewed and discussedbefore publication [3, 21. The journal Agricell Report (vol. 25, p. 21, 1995) relieved the main observations and data allowing our definition. This definition, at the cellular level, implies an array of characteristics (as summarized in ruble I), for an exceptional plant cell line examined under biological. morphological and biochemical view angles. All these characteristics are those of animal metastases,including: close to full hormone independence, polyploidy and aneuploidy 141,complete loss of cell-to-cell adhesion (here essentially due to an over-esterification of pectin [7]), permanent oxidative stress [5] and accumulation of polyamines [6]. Plant cancer cells eviPlant
Physiol.
B&hem..
098 l-9428/98/03/0
Elsevier,
Paris.
dently cannot become circulating metastases (or “extra cells” [ 11).But becausenormal plant cells have the unique capacity (animal cells do not) to organize themselves into organogenic or regenerating meristems,the typical plant cancer trait has been precisely defined as the irreversible loss of organogenic totipotency, i.e. the capacity for such cells to reorganize primary organogenic meristemsat the end of a neoplastic progression. This definition makes a clear distinction with tumours (such as mediated by pathogens, or resulting of genetic transformation [I]) which are chimerit and still organogenic. Similarly bud- and meristem-bearing shoots in culture may loose their totipotency along a neoplastic progression (involving vitrification and habituation successively), where all the characteristics reported in table I will appear progressively. The rooting capacity will be lost first with the acquisition of hormonal independence, and therefore the unsensitivity to the exogenous rooting auxin; appearanceof stem fasciation will be the first sign of stem me&em disfunctioning; increasing “breakability” (resulting from loss of cellto-cell adhesion, ... and communication) will necessarily be followed by necroses of apices (caulogenic meristems) and meristematic leaf borders. When synchronized, these necroseshave been considered [3, 21 as the sign of generalized cancer induced death of the whole organism. Notice that the non-meristematic cells still surviving in contact with the culture medium
204
T. Gaspar
Table
I. Characteristics which led to consider a fully habituated nonorganonogenic sugarbeet callus as made of true cancerous cells (in the absence of pathogens).
Biological - monoclonal
characteristics
origin - full hormonal independence ~ high rate of cell division polyploidy and aneuploidy - reduced cell-to-cell adhesion - susceptibility to necrosis
Morphological -
REFERENCES
(friability)
characteristics
deficient cell wall differentiation deficient chloroplast and mitochondria large nuclei with irregular shape, with apoptotic bodies
Biochemical -
in vitro
differentiation many nucleoli
+ micronuclei
compounds
Typical plant cancer trait - irreversible loss of organogenic cells to reorganize plastic progression.
primary
[l] DoonanJ., Hunt T., Why don’tplantsget cancer? Nature 380(1996)481-482. [2] GasparTh., The conceptof cancerin in vitro plant culturesand the implicationof habituationto hormonesand hyperhydricity, Plant TissueCult. Biotechn. 1 (1995) 126-136. [3] Gaspar Th., Hagege D.. Kevers C., Penel C., Creve-
characteristics
programmed cell death’! hyperhydricity deficiency of tetrapyrrole-containing permanent oxidative stress low ethylene production accumulation of polyamines
features are simply different. This has been partly expressed by Doonan and Hunt [I] in their article, where they write that plants, contrarily to animals, incorporate extra cells into the normal body plan... but the body might be only apparently normal... and not at the end of the neoplastic progression.
totipotency, i.e. the capacity for such organogenic meristems at the end of a neo-
may continue to form extra cancerous cells and grow into a fully habituated nonorganogenic callus. I have not insisted on stressing the factors of some in vitro plant cultures which may lead to such cancer cases; this was to say that plants were probably no more resistant to neoplastic transformation than animals. the
coeurM., Engelmann I., Greppin H., Foidart J. M., When plant teratomasturn into cancersin the absenceof pathogens,Physiol. Plant. 83 (199I) 696-701. ]4] HagegeD., CataniaR., Micalef H., GasparTh., Nuclear shapeand DNA content of fully habituatednonorganogeniesugarbeetcells,Protoplasma166(1992)49-54. [S] KeversC., BisbisB., Le Dily F., Billard J. P..Huault C., Gaspar Th., Darkness improves growth and delays necrosisin a non chlorophyllous habituatedsugarbeet callus,In Vitro Cell. Dev.Biol. 3 1 ( 1995)12-l 26. [6] Le Dily F.,Billard J. P.,GasparTh., HuaultC., Disturbed nitrogen metabolismassociatedwith the hyperhydric statusof fully habituatedcallus of sugarbeet,Physiol. Plant. 88 (1993) 129-134. [7] Liners F., Gaspar Th.. Van Cutsem, P., Acetyl- and methyl-esterificationof pectinsof friable and compact sugar-beet calli: consequences for intercellularadhesion, Planta192(1994)545-556.
Biochrm..
1998.
36 (3),
203-204
Letter to the Editor Plants can get cancer Thomas
Gaspar
lnstitut de Botanique B 22, UniversitC de Libge, Sart Tilman, B-4000 Libge. Belgique (Tel./Fax 32-4-366 38 59) (Received July 15, 1997: accepted September 29, 1997)
Abstract - This is a reply to a paper entitled “Why don’t plants get cancer”, with an opposite opinion, and with arguments. Although there are many similitudes betwen animal and plant cancerous cells and organisms, because plant cancerous cells cannot become circulating metastases, plant cancer at the end of a neoplastic progression has needed a specific definition. The typical plant cancer trait is the irreversible loss of organogenic totipotency, i.e. the capacity of cancerous cells to reorganize primary organogenic meristems. 0 Elsevier, Paris. Plant cancer / organogenic
totipotency
I reply to a paper entitled “Why don’t plants get cancer?‘, published by Doonan and Hunt [I], because I am convinced of the contrary. Is the divergence a simple question of concept? I have been working for fifteen years on the processesof habituation (loss of requirement of exogenous growth regulators for sustained growth in vitro) and vitrification (hyperhydric malformations) of in vitro cultured cells and shoots respectively. I came to the conclusion that both phenomena were taking part in neoplastic progressions (in the absence of pathogens), leading to true cancer cells (in calli) or to true generalized cancers at the organismic (shoot) level, with (programmed?) death as ultimate issues. I summarize herewith the arguments developed for such plant cancer concepts which where pre-reviewed and discussedbefore publication [3, 21. The journal Agricell Report (vol. 25, p. 21, 1995) relieved the main observations and data allowing our definition. This definition, at the cellular level, implies an array of characteristics (as summarized in ruble I), for an exceptional plant cell line examined under biological. morphological and biochemical view angles. All these characteristics are those of animal metastases,including: close to full hormone independence, polyploidy and aneuploidy 141,complete loss of cell-to-cell adhesion (here essentially due to an over-esterification of pectin [7]), permanent oxidative stress [5] and accumulation of polyamines [6]. Plant cancer cells eviPlant
Physiol.
B&hem..
098 l-9428/98/03/0
Elsevier,
Paris.
dently cannot become circulating metastases (or “extra cells” [ 11).But becausenormal plant cells have the unique capacity (animal cells do not) to organize themselves into organogenic or regenerating meristems,the typical plant cancer trait has been precisely defined as the irreversible loss of organogenic totipotency, i.e. the capacity for such cells to reorganize primary organogenic meristemsat the end of a neoplastic progression. This definition makes a clear distinction with tumours (such as mediated by pathogens, or resulting of genetic transformation [I]) which are chimerit and still organogenic. Similarly bud- and meristem-bearing shoots in culture may loose their totipotency along a neoplastic progression (involving vitrification and habituation successively), where all the characteristics reported in table I will appear progressively. The rooting capacity will be lost first with the acquisition of hormonal independence, and therefore the unsensitivity to the exogenous rooting auxin; appearanceof stem fasciation will be the first sign of stem me&em disfunctioning; increasing “breakability” (resulting from loss of cellto-cell adhesion, ... and communication) will necessarily be followed by necroses of apices (caulogenic meristems) and meristematic leaf borders. When synchronized, these necroseshave been considered [3, 21 as the sign of generalized cancer induced death of the whole organism. Notice that the non-meristematic cells still surviving in contact with the culture medium
204
T. Gaspar
Table
I. Characteristics which led to consider a fully habituated nonorganonogenic sugarbeet callus as made of true cancerous cells (in the absence of pathogens).
Biological - monoclonal
characteristics
origin - full hormonal independence ~ high rate of cell division polyploidy and aneuploidy - reduced cell-to-cell adhesion - susceptibility to necrosis
Morphological -
REFERENCES
(friability)
characteristics
deficient cell wall differentiation deficient chloroplast and mitochondria large nuclei with irregular shape, with apoptotic bodies
Biochemical -
in vitro
differentiation many nucleoli
+ micronuclei
compounds
Typical plant cancer trait - irreversible loss of organogenic cells to reorganize plastic progression.
primary
[l] DoonanJ., Hunt T., Why don’tplantsget cancer? Nature 380(1996)481-482. [2] GasparTh., The conceptof cancerin in vitro plant culturesand the implicationof habituationto hormonesand hyperhydricity, Plant TissueCult. Biotechn. 1 (1995) 126-136. [3] Gaspar Th., Hagege D.. Kevers C., Penel C., Creve-
characteristics
programmed cell death’! hyperhydricity deficiency of tetrapyrrole-containing permanent oxidative stress low ethylene production accumulation of polyamines
features are simply different. This has been partly expressed by Doonan and Hunt [I] in their article, where they write that plants, contrarily to animals, incorporate extra cells into the normal body plan... but the body might be only apparently normal... and not at the end of the neoplastic progression.
totipotency, i.e. the capacity for such organogenic meristems at the end of a neo-
may continue to form extra cancerous cells and grow into a fully habituated nonorganogenic callus. I have not insisted on stressing the factors of some in vitro plant cultures which may lead to such cancer cases; this was to say that plants were probably no more resistant to neoplastic transformation than animals. the
coeurM., Engelmann I., Greppin H., Foidart J. M., When plant teratomasturn into cancersin the absenceof pathogens,Physiol. Plant. 83 (199I) 696-701. ]4] HagegeD., CataniaR., Micalef H., GasparTh., Nuclear shapeand DNA content of fully habituatednonorganogeniesugarbeetcells,Protoplasma166(1992)49-54. [S] KeversC., BisbisB., Le Dily F., Billard J. P..Huault C., Gaspar Th., Darkness improves growth and delays necrosisin a non chlorophyllous habituatedsugarbeet callus,In Vitro Cell. Dev.Biol. 3 1 ( 1995)12-l 26. [6] Le Dily F.,Billard J. P.,GasparTh., HuaultC., Disturbed nitrogen metabolismassociatedwith the hyperhydric statusof fully habituatedcallus of sugarbeet,Physiol. Plant. 88 (1993) 129-134. [7] Liners F., Gaspar Th.. Van Cutsem, P., Acetyl- and methyl-esterificationof pectinsof friable and compact sugar-beet calli: consequences for intercellularadhesion, Planta192(1994)545-556.