A Young Seedling Stripe2 phenotype in rice is caused by mutation of a chloroplast-localized nucleoside diphosphate kinase 2 required for chloroplast biogenesis

Abstract

Chloroplast development and chlorophyll (Chl) biosynthesis in plants are regulated by many genes, but the underlying molecular mechanisms remain largely elusive. We isolated a rice mutant named yss2 (young seedling stripe2) with a striated seedling phenotype beginning from leaf 2 of delayed plant growth. The mutant developed normal green leaves from leaf 5, but reduced tillering and chlorotic leaves and panicles appeared later. Chlorotic yss2 seedlings have decreased pigment contents and impaired chloroplast development. Genetic analysis showed that the mutant phenotype was due to a single recessive gene. Positional cloning and sequence analysis identified a single nucleotide substitution in YSS2 gene causing an amino acid change from Gly to Asp. The YSS2 allele encodes a NDPK2 (nucleoside diphosphate kinase 2) protein showing high similarity to other types of NDPKs. Real-time RT-PCR analysis demonstrated that YSS2 transcripts accumulated highly in L4 sections at the early leaf development stage. Expression levels of genes associated with Chl biosynthesis and photosynthesis in yss2 were mostly decreased, but genes involved in chloroplast biogenesis were up-regulated compared to the wild type. The YSS2 protein was associated with punctate structures in the chloroplasts of rice protoplasts. Our overall data suggest that YSS2 has important roles in chloroplast biogenesis.

Nucleotide Metabolism in Plants

“…The NDPKs are multisubstrate enzymes accepting all nucleoside/deoxynucleoside diphosphates (Zrenner et al, 2006), but there is a preference for generating GTP (Kihara et al, 2011), which in the chloroplast may assist in repairing photosystem II (Spetea and Lundin, 2012). Mutation of the gene for the plastidic NDPK in rice results in a pale green phenotype and a lower photosynthetic rate (Ye et al, 2016;Zhou et al, 2017), but since the chloroplast function is partially retained, there also must be nucleoside triphosphate import into this organelle. Interestingly, NDPKs can also have moonlighting activity as modulators of gene expression (Dorion and Rivoal, 2018).…”

UMP Kinase Regulates Chloroplast Development and Cold Response in Rice

“…These decreases suggest that the mutation of UMPK affected the pyrimidine synthesis and the influence was greater on the direct product UDP than on the indirect product UTP. Expression analyses were performed for UMPK and another gene, OsNDPK2 , which encodes the nucleoside diphosphate kinase that phosphorylates UDP to form UTP [4,5] (Figure 2b). The two genes exhibited higher expression levels in the mutant, more than twice those in the WT.…”

“…Three other genes involved in nucleotide metabolism were also found to regulate PEP activity. They included OsNDPK2 [5]; ATase2 encoding glutamine phosphoribosyl pyrophosphate amidotransferase that catalyzes the first step of purine biosynthesis [26]; and GARS encoding a glycinamide ribonucleotide synthetase that catalyzes the second step of purine biosynthesis [33]. In mutants of these genes, the expression of PEP-dependent genes was consistently down-regulated.…”

“…OsNDPK2 encodes a nucleoside diphosphate kinase in the nucleotide inter-conversion pathway, which catalyzes the phosphorylation of NDP to form NTP. Mutation of OsNDPK2 impaired chloroplast development and increased sensitivity to salinity stress [4,5]. ST2 / ALR encodes a dCMP deaminase in the nucleotide inter-conversion pathway, which catalyzes dCMP to dUMP.…”

PUMPKIN, the Sole Plastid UMP Kinase, Associates with Group II Introns and Alters Their Metabolism

“…Evolutionary conserved eubacterial UMP kinases are essential homohexamers and catalyze the reversible transfer of the c-phosphoryl group from ATP to UMP to yield UDP (Serina et al, 1995;Kafer et al, 2004). UDP is further phosphorylated to UTP in an additional ATP consuming reaction by the nucleoside diphosphate kinase (Zhou et al, 2017). Cellular pyrimidine metabolism is primarily important for the synthesis of RNA as well as galacto-and sulfolipids through UDP-sugars (Zrenner et al, 2006;Okazaki et al, 2009).…”