The Senescence-Induced Staygreen Protein Regulates Chlorophyll Degradation

Abstract

Loss of green color in leaves results from chlorophyll (Chl) degradation in chloroplasts, but little is known about how Chl catabolism is regulated throughout leaf development. Using the staygreen (sgr) mutant in rice (Oryza sativa), which maintains greenness during leaf senescence, we identified Sgr, a senescence-associated gene encoding a novel chloroplast protein. Transgenic rice overexpressing Sgr produces yellowish-brown leaves, and Arabidopsis thaliana pheophorbide a oxygenase-impaired mutants exhibiting a stay-green phenotype during dark-induced senescence have reduced expression of Sgr homologs, indicating that Sgr regulates Chl degradation at the transcriptional level. We show that the leaf staygreenness of the sgr mutant is associated with a failure in the destabilization of the light-harvesting chlorophyll binding protein (LHCP) complexes of the thylakoid membranes, which is a prerequisite event for the degradation of Chls and LHCPs during senescence. Transient overexpression of Sgr in Nicotiana benthamiana and an in vivo pull-down assay show that Sgr interacts with LHCPII, indicating that the Sgr-LHCPII complexes are formed in the thylakoid membranes. Thus, we propose that in senescing leaves, Sgr regulates Chl degradation by inducing LHCPII disassembly through direct interaction, leading to the degradation of Chls and Chl-free LHCPII by catabolic enzymes and proteases, respectively.

Stay-green protein, defective in Mendel’s green cotyledon mutant, acts independent and upstream of pheophorbide a oxygenase in the chlorophyll catabolic pathway

“…In addition, core subunits of PSI (PsaD) and PSII (PsbA) were also retained to some extend in the mutant, and degradation of Rubisco subunits was somewhat slower in JI2775 compared to JI4. Together these data confirm earlier observations of high LHCII retention in stay-green mutants (Hilditch et al, 1989;Jiang et al, 2007;Park et al, 2007).…”

“…3A, B). LHCII was fully retained during the course of senescence in JI2775, a feature that has been described in different stay-green mutants (Hilditch et al, 1989;Bachmann et al, 1994;Pružinská et al, 2003;Park et al, 2007), but in contrast to the stay-green mutant Bf993 of Festuca pratensis (Thomas and Howarth, 2000), proteolytic fragments of LHCII could not be detected in JI2775. In addition, core subunits of PSI (PsaD) and PSII (PsbA) were also retained to some extend in the mutant, and degradation of Rubisco subunits was somewhat slower in JI2775 compared to JI4.…”

“…Along with the retention of chl, chl-binding proteins were shown to be retained in the mutants (Hilditch et al, 1989;Jiang et al, 2007;Park et al, 2007;Sato et al, 2007). Recently, it was demonstrated that rice SGR is able to specifically interact with LHCII subunits (Park et al, 2007). This together with the retention of these proteins in the mutants, suggested that SGR might be involved in dismantling chl-protein complexes as a prerequisite for both chl and apoprotein degradation.…”

“…These mutants are defective in a gene identified in the Bf993 mutant of Festuca pratensis (Thomas, 1987). The gene was termed SID (senescenceinduced degradation), but orthologous genes from rice, pea and Arabidopsis have now been designated SGR (STAY-GREEN) (Jiang et al, 2007;Park et al, 2007;Sato et al, 2007), SGN (Park et al, 2007) or NYE1 (nonyellowing) (Ren et al, 2007).…”

“…It was argued that pheide a accumulation would feed back inhibit chl breakdown, in order to prevent further chl intermediate accumulation, thereby minimizing the phototoxic potential of these pigments (Thomas, 1997;Matile et al, 1999;Hörtensteiner, 2006). Along with the retention of chl, chl-binding proteins were shown to be retained in the mutants (Hilditch et al, 1989;Jiang et al, 2007;Park et al, 2007;Sato et al, 2007). Recently, it was demonstrated that rice SGR is able to specifically interact with LHCII subunits (Park et al, 2007).…”