Poly(ADP‐ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance

Abstract

SummaryPlants contain two genes that code for poly(ADP-ribose) polymerase (PARP): parp1 and parp2. Both PARPs are activated by DNA damage caused by, example reactive oxygen species. Upon activation polymers of ADPribose are synthesized on a range of nuclear enzymes using NAD + as substrate. Here, we show that in plants stresses such as drought, high light and heat activate PARP causing NAD + breakdown and ATP consumption.When the PARP activity is reduced by means of chemical inhibitors or by gene silencing, cell death is inhibited and plants become tolerant to a broad range of abiotic stresses like high light, drought and heat. Plant lines with low poly(ADP-ribosyl)ation activity maintain under stress conditions their energy homeostasis by reducing NAD + breakdown and consequently energy consumption. The higher energy-use efficiency avoids the need for a too intense mitochondrial respiration and consequently reduces the formation of reactive oxygen species. From these results it can be concluded that breeding or engineering for a high energy-use efficiency under stress conditions is a valuable, but until today nearly unexploited, approach to enhance overall stress tolerance of crops.

The Paralogous GenesRADICAL-INDUCED CELL DEATH1andSIMILAR TO RCD ONE1Have Partially Redundant Functions during Arabidopsis Development

“…Orthologs of PARP-1 and PARP-2, the DNA-dependent PARPs, AtPARP1 (At4g02390) and AtPARP2 (At2g31320), respectively, have been identified (Lepiniec et al, 1995;Babiychuk et al, 1998). These genes have been implicated in DNA repair (Doucet-Chabeaud et al, 2001;De Block et al, 2005) and have been shown to be associated with chromosomes through their N-terminal zinc fingers (Babiychuk et al, 2001). AtPARP1 and AtPARP2 are up-regulated during geminivirus infection, most likely in response to accumulation of nicked viral DNA forms (Ascencio-Ibanez et al, 2008), and also accumulate under conditions of DNA stress (Culligan et al, 2006).…”

“…PARP inhibitor studies have demonstrated the involvement of PARPs in abiotic stress (Amor et al, 1998;De Block et al, 2005) and defense responses (Berglund et al, 1996;Adams-Phillips et al, 2008). A role for PARP activity in seeds to protect against genotoxic stress has also been inferred (Hunt and Gray, 2009).…”

Abiotic stress and the plant circadian clock

“…85 PARP reaction consumes NAD and ATP, therefore affecting energy homeostasis. 86 These authors observed that the downregulation of PARP enhanced stress tolerance probably due to a reduced consumption of NAD and ATP. However Vanderauwera et al suggested an alternative hypothesis in which the downregulation of PARP activity caused plants to display abiotic stress tolerance due to induction of ABA responsive and ABA signaling genes and not through the direct consumption of energy (NAD and ATP).…”

Mutation of OsNaPRT1 in the NAD Salvage Pathway Leads to Withered Leaf Tips in Rice

“…On the other hand, new functions of NAD and its derivatives in the salvage pathway have been found involving the regulation of complex cellular processes, including transcriptional regulation via NADdependent deacetylation and poly(ADP-ribosylation) (Imai et al, 2000;North et al, 2003;Sánchez et al, 2004;De Block et al, 2005). For instance, NAD can be broken down into nicotinamide by silent information regulator 2 (SIR2) and poly(ADP-ribose)polymerase.…”

“…There is increasing evidence that the biosynthesis, degradation, and recycling of NAD(P)(H) are associated with signal transduction, developmental regulation, and stress resistance (Amor et al, 1998;Imai et al, 2000;North et al, 2003;Mittler et al, 2004;Sánchez et al, 2004;Chai et al, 2005Chai et al, , 2006De Block et al, 2005). The amount of NAD(P)(H) should be sufficient for preventing cell death due to NAD depletion in vivo.…”