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Commun Integr Biol. 2010 Sep-Oct; 3(5): 468–470.
PMCID: PMC2974083

Catechin secretion and phytotoxicity

Fact not fiction

Abstract

Research indicates that the invasiveness of Centaurea stoebe is attributed to the stronger allelopathic effects on the native North American species than on the related European species, which is one of the unquestionable aspects of the “novel weapons hypothesis (NWH).” Studies originating from controlled to field conditions have shown that C. stoebe utilizes its biochemical potential to exert its invasiveness. The roots of C. stoebe secrete a potent phytotoxin, catechin, which has a detrimental effect on the surrounding plant species. Although, studies on catechin secretion and phytotoxicity represent one of the most well studied systems describing negative plant-plant interactions, it has also sparked controversies lately due to its phytotoxicity dosages and secretion effluxes. Previous reports negate the phytotoxic and pro-oxidant nature of catechin.13 In our recent study we have shown that catechin is highly phytotoxic against Arabidopsis thaliana and Festuca idahoensis. We also show that (±) catechin applied to roots of A. thaliana induces reactive oxygen species (ROS) confirming the pro-oxidant nature of catechin. In addition, activation of signature cell death genes such as acd2 and cad1 post catechin treatment in A. thaliana ascertains the phytotoxic nature of catechin.

Key words: Catechin, allelopathy, root secretion, ROS, Centaurea

The secretion of catechin from the roots of the noxious weed, Centaurea stoebe is one of the best described examples of negative plant-plant interactions mediated through phytotoxins, which is also known as allelopathy.4 In the last eight years, various lines of research have shown that different invasive plants use a biochemical machinery to target recipient plant communities to invade in direct and indirect plant-plant interactions.4 It has been demonstrated that when applied to the roots of Arabidopsis thaliana, the phytotoxin (±) catechin triggers a wave of reactive oxygen species (ROS), leading to a cascade of genome-wide changes in gene expression and, ultimately, death of the root system.5 Biochemical links describing the root secreted phytotoxin, (±) catechin, represent one of the most well studied systems to describe negative plant-plant interactions. However, the original work on catechin has also sparked some controversies on phytotoxicity and pro-oxidant behavior of the secreted chemical. Earlier studies13 showed that catechin is not phytotoxic but it bears strong anti-oxidant activity. To add to this inconsistency, one of the original reports of catechin secretion has been recently retracted from the literature.6 The retracted note conveys that the authors of the original report failed to reproduce catechin secretion and phytotoxicity against Arabidopsis thaliana. In contrast, several other lines of work,723 some originating from the same research group showed catechin secretion to an order of mg g−1 samples.5,7,14,15,18,20 It is valid to argue that the irreproducibility in catechin secretion observed by Stermitz et al. (2009)6 could be related to the factors such as instability of catechin in medium and sampling time. Since, Stermitz et al. (2009)6 didn't dwell on the methodological difficulties that were encountered negating the detection of catechin in their repetition trials; it is hard to explain how the same group5,7,14,15,18,20 reported catechin in the secretions of C. stoebe to a level of mg g−1 sample. In contrast, our recent data24 clearly shows that catechin is indeed phytotoxic against A. thaliana and Festuca idahoensis. Duke et al. 2009 were unable to replicate the phytotoxicity studies from previous reports5 mainly due to the fact that they did not follow the exact procedure as described by Bais et al. 2003. They used 3 seedlings per treatment versus one seedling per treatment. In addition, they used acetone as a solvent instead of methanol5 and used half strength MS medium in place of full strength. These differences, though seemingly trivial were enough to cause discrepancies in the data as elaborated in our results.24 Our data showed a clear enantiomeric dependent affect of (±) catechin, wherein (−) catechin isomer revealed a severe rhizotoxic response at 20 µgml−1 level.24 Root mortality patterns were also checked by time lapse movies, wherein seedlings treated with (±) catechin (100 µgml−1), (−) catechin (10 µgml−1) and (+) catechin (200–250 µgml−1) were transferred on day 3 to MS plates without any catechins. Our recent time lapse movies show that seedlings treated with (−) catechin show strong mortality (as documented by no or reduced root growth) compared to (+) catechin isomer treated roots.24 In addition, the phytotoxic effect was manifested equally in aqueous as well as organic phase against both A. thaliana and F. idahoensis. Interestingly, our data also revealed the presence of catechin in the growth medium of C. stoebe to support a recent study.21 The authors reported high levels of catechin secretion from C. stoebe hydroponic cultures compared to previous reports.1 Interestingly, these authors also reported that catechin secretion in C. stoebe is diurnally regulated; wherein catechin degrades to catechol. Our results were concurrent with these findings indicating that the time of sampling could be an issue in detection of catechin. Furthermore, the unstable nature of the compound also adds to the variations in its detection and quantification.

Our original report that the phytotoxicity of catechin treated roots is prompted by elevated levels of ROS was corroborated by the fact that catechin treatment results in the production of elevated levels of ROS.2530 The argument that catechins bear a strong anti-oxidant activity3 is not very exciting, as catechins are reported anti-oxidants (SciFinder search as October 2008). However, the inference drawn by Duke et al. (2009) that catechins cannot bear pro-oxidant activity because they are anti-oxidants might be a little premature especially since the anti- and pro-oxidant capacity is correlated to the number of hydroxyl groups.2528 Likewise, Sofic et al. (2001) have reported that anti to prooxidant shifts of catechins might be attributed to their hydroxyl and amine groups.28

Furthermore, we showed that catechin phytotoxicity is mediated through transcriptional upregulation of signature cell death genes such as accelerated cell death (acd2) and constitutively activated cell death 1 (cad1). We also reconfirmed the earlier observation that catechin induces reactive oxygen mediated (ROS) mediated phytotoxicity in A. thaliana and that catechin induced ROS is aggravated in presence of divalent transition metals. Catechin is known to bind to transition elements to enhance its phytotoxicity and conditional allelopathic response.17 This supports our observation that ROS due to catechin-metal complex is responsible for modification of downstream signaling proteins contributing to altered gene expression and cell death.

While our results advocate the phytotoxic and pro-oxidant nature of catechin, they also highlight the fact that this allelochemical may be perceived differently by plant communities when they are in monocultures versus isolated stands. The deviation in results reported previously13 could be due to different media conditions and a group effect in catechin treated seedlings. Our data proposes that precise conditions are needed to evaluate the overall effect of catechin secretion and toxicity.

Footnotes

References

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