DNA damage and repair in plants - from models to crops

Abstract

The genomic integrity of every organism is constantly challenged by endogenous and exogenous DNA-damaging factors. Mutagenic agents cause reduced stability of plant genome and have a deleterious effect on development, and in the case of crop species lead to yield reduction. It is crucial for all organisms, including plants, to develop efficient mechanisms for maintenance of the genome integrity. DNA repair processes have been characterized in bacterial, fungal, and mammalian model systems. The description of these processes in plants, in contrast, was initiated relatively recently and has been focused largely on the model plant Arabidopsis thaliana. Consequently, our knowledge about DNA repair in plant genomes - particularly in the genomes of crop plants - is by far more limited. However, the relatively small size of the Arabidopsis genome, its rapid life cycle and availability of various transformation methods make this species an attractive model for the study of eukaryotic DNA repair mechanisms and mutagenesis. Moreover, abnormalities in DNA repair which proved to be lethal for animal models are tolerated in plant genomes, although sensitivity to DNA damaging agents is retained. Due to the high conservation of DNA repair processes and factors mediating them among eukaryotes, genes and proteins that have been identified in model species may serve to identify homologous sequences in other species, including crop plants, in which these mechanisms are poorly understood. Crop breeding programs have provided remarkable advances in food quality and yield over the last century. Although the human population is predicted to "peak" by 2050, further advances in yield will be required to feed this population. Breeding requires genetic diversity. The biological impact of any mutagenic agent used for the creation of genetic diversity depends on the chemical nature of the induced lesions and on the efficiency and accuracy of their repair. More recent targeted mutagenesis procedures also depend on host repair processes, with different pathways yielding different products. Enhanced understanding of DNA repair processes in plants will inform and accelerate the engineering of crop genomes via both traditional and targeted approaches.

Keywords: Arabidopsis; DNA damage; DNA repair; crop plants; mutagenesis.

FIGURE 1

Schematic representation of the major DNA lesions induced by various external and endogenous factors, and the types of DNA repair mechanisms employed to remove them from the eukaryotic genome.

FIGURE 2

Schematic representation of the photoreactivation mechanism utilized by plants to repair UV-induced pyrimidine dimers. On the left is schematized the classical well characterized process of CPD photoreactivation in double-stranded DNA. On the right is presented a hypothetical mode of CPD photoreactivation, which might operate within the open DNA regions generated during transcription, replication and repair processes. It is thought to bemediated by the DASH chryptochromes, based on their ability to photoreactivate CPD in single-stranded DNA (Pokorny et al., 2008). Future research is needed to prove or reject such an intriguing concept. T/R/R complex – transcription, replication or repair complex.

FIGURE 3

Schematic representation of GGR and TCR in the eukaryotic cells. Two main concepts exist regarding the fate of stalled RP. According to the first model, after completion of repair, the transcription continues from the point it has been impaired without degradation of RNA Pol II and its nascent transcript; a key role in this step is attributed to the elongation factor ELL which is thought to help the backtracked RNA pol II to release from chromatin as well as to attract additional, yet unidentified factors allowing transcription restart (Mourgues et al., 2013). Another possibility is that the stalled polymerase and its growing transcript are released from DNA and further degraded; the lesion is removed and transcription starts by new RNA pol II complexes from the beginning of the gene on an intact damage-free template (Sarasin and Stary, 2007).

FIGURE 4

Diagrammatic representation of the DSB inducing factors and the various damage recognition and repair pathways.