Cryptic chlorophyll breakdown in non-senescent green Arabidopsis thaliana leaves
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Chlorophyll (Chl) breakdown is a diagnostic visual process of leaf senescence, which furnishes phyllobilins (PBs) by the PAO/phyllobilin pathway. As Chl breakdown disables photosynthesis, it appears to have no role in photoactive green leaves. Here, colorless PBs were detected in green, non-senescent leaves of Arabidopsis thaliana. The PBs from the green leaves had structures entirely consistent with the PAO/phyllobilin pathway and the mutation of a single Chl catabolic enzyme completely abolished PBs with the particular modification. Hence, the PAO/phyllobilin pathway was active in the absence of visible senescence and expression of genes encoding Chl catabolic enzymes was observed in green Arabidopsis leaves. PBs accumulated to only sub-% amounts compared to the Chls present in the green leaves, excluding a substantial contribution of Chl breakdown from rapid Chl turnover associated with photosystem II repair. Indeed, Chl turnover was shown to involve a Chl a dephytylation and Chl a reconstitution cycle. However, non-recyclable pheophytin a is also liberated in the course of photosystem II repair, and is proposed here to be scavenged and degraded to the observed PBs. Hence, a cryptic form of the established pathway of Chl breakdown is indicated to play a constitutive role in photoactive leaves.
KeywordsChlorophyll breakdown Chlorophyll turnover PAO/phyllobilin pathway Pheophytin Phyllobilin Photosystem II repair
This work was supported by Austrian Science Fund (FWF, Project P-28522 to B.K.) and the Swiss National Foundation (Project 31003A_172977 to S.H.).
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Conflict of interest
The authors declare that they have no conflict of interest.
- Chew AG, Bryant DA (2007) Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. Annu Rev Microbiol 61:113–129. https://doi.org/10.1146/annurev.micro.61.080706.093242 CrossRefGoogle Scholar
- Christ B, Schelbert S, Aubry S, Süssenbacher I, Müller T, Kräutler B, Hörtensteiner S (2012) MES16, a member of the methylesterase protein family, specifically demethylates fluorescent chlorophyll catabolites during chlorophyll breakdown in Arabidopsis. Plant Physiol 158:628–641. https://doi.org/10.1104/pp.111.188870 CrossRefGoogle Scholar
- Christ B, Egert A, Süssenbacher I, Kräutler B, Bartels D, Peters S, Hörtensteiner S (2014) Water deficit induces chlorophyll degradation via the ‘PAO/phyllobilin’ pathway in leaves of homoio- (Craterostigma pumilum) and poikilochlorophyllous (Xerophyta viscosa) resurrection plants. Plant Cell Environ 37:2521–2531CrossRefGoogle Scholar
- Gray J, Wardzala E, Yang M, Reinbothe S, Haller S, Pauli F (2004) A small family of LLS1-related non-heme oxygenases in plants with an origin amongst oxygenic photosynthesizers. Plant Mol Biol 54:39–54. https://doi.org/10.1023/B:PLAN.0000028766.61559.4c CrossRefGoogle Scholar
- Heyes DJ, Hunter CN (2008) Biosynthesis of chlorophyll and bacteriochlorophyll. In: Warren MJ, Smith AG (eds) Tetrapyrroles: birth, life and death. Landes Bioscience, Austin, pp 233–247Google Scholar
- Hörtensteiner S, Vicentini F, Matile P (1995) Chlorophyll breakdown in senescent cotyledons of rape, Brassica napus L.: enzymatic cleavage of phaeophorbide a in vitro. New Phytol 129:237–246. https://doi.org/10.1111/j.1469-8137.1995.tb04293.x CrossRefGoogle Scholar
- Kräutler B, Hörtensteiner S (2014) Chlorophyll breakdown: chemistry, biochemistry and biology. In: Ferreira GC, Kadish KM, Smith KM, Guilard R (eds) Handbook of porphyrin science—chlorophyll, photosynthesis and bio-inspired energy, vol 28. Handbook of porphyrin science, vol 28. World Scientific Publishing, Singapore, pp 117–185. https://doi.org/10.1142/9789814407755_0021
- Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136. https://doi.org/10.1146/annurev.arplant.57.032905.105316 CrossRefGoogle Scholar
- Mittelberger C et al (2017) Pathogen-induced leaf chlorosis: products of chlorophyll breakdown found in degreened leaves of Phytoplasma-infected apple (Malus x domestica Borkh.) and spricot (Prunus armeniaca L.) trees relate to the pheophorbide a oxygenase/phyllobilin pathway. J Agric Food Chem 65:2651–2660. https://doi.org/10.1021/acs.jafc.6b05501 CrossRefGoogle Scholar
- Mühlecker W, Kräutler B (1996) Breakdown of chlorophyll: constitution of nonfluorescing chlorophyll-catabolites from senescent cotyledons of the dicot rape. Plant Physiol Biochem 34:61–75Google Scholar
- Nickelsen J, Rengstl B (2013) Photosystem II assembly: from cyanobacteria to plants. Annu Rev Plant Biol 64:609–635. https://doi.org/10.1146/annurev-arplant-050312-120124 CrossRefGoogle Scholar
- Oberhuber M, Berghold J, Breuker K, Hörtensteiner S, Kräutler B (2003) Breakdown of chlorophyll: a nonenzymatic reaction accounts for the formation of the colorless “nonfluorescent” chlorophyll catabolites. Proc Natl Acad Sci USA 100:6910–6915. https://doi.org/10.1073/pnas.1232207100 CrossRefGoogle Scholar
- Süssenbacher I, Hörtensteiner S, Kräutler B (2015a) A dioxobilin-type fluorescent chlorophyll catabolite as a transient early intermediate of the dioxobilin-branch of chlorophyll breakdown in Arabidopsis thaliana. Angew Chem Int Ed 54:13777–13781. https://doi.org/10.1002/anie.201506299 CrossRefGoogle Scholar