Chloroplastic Phosphoadenosine Phosphosulfate Metabolism Regulates Basal Levels of the Prohormone Jasmonic Acid in Arabidopsis Leaves

Abstract

Levels of the enzymes that produce wound response mediators have to be controlled tightly in unwounded tissues. The Arabidopsis (Arabidopsis thaliana) fatty acid oxygenation up-regulated8 ( fou8) mutant catalyzes high rates of a-linolenic acid oxygenation and has higher than wild-type levels of the a-linolenic acid-derived wound response mediator jasmonic acid (JA) in undamaged leaves. fou8 produces a null allele in the gene SAL1 (also known as FIERY1 or FRY1). Overexpression of the wild-type gene product had the opposite effect of the null allele, suggesting a regulatory role of SAL1 acting in JA synthesis. The biochemical phenotypes in fou8 were complemented when the yeast (Saccharomyces cerevisiae) sulfur metabolism 3#(2#), 5#-bisphosphate nucleotidase MET22 was targeted to chloroplasts in fou8. The data are consistent with a role of SAL1 in the chloroplast-localized dephosphorylation of 3#-phospho-5#-adenosine phosphosulfate to 5#-adenosine phosphosulfate or in a closely related reaction (e.g. 3#,5#-bisphosphate dephosphorylation). Furthermore, the fou8 phenotype was genetically suppressed in a triple mutant ( fou8 apk1 apk2) affecting chloroplastic 3#-phospho-5#-adenosine phosphosulfate synthesis. These results show that a nucleotide component of the sulfur futile cycle regulates early steps of JA production and basal JA levels.

Phosphate Deficiency Induces the Jasmonate Pathway and Enhances Resistance to Insect Herbivory

“…Potassium deficiency in Arabidopsis increased the expression of several JA-responsive genes, enhanced the synthesis of several oxylipins in leaves, including JA, and was associated with reduced damage by thrips (Armengaud et al, 2004Troufflard et al, 2010). Sulfur deficiency resulted in an enhanced expression of several genes involved in JA synthesis, and mutation affecting sulfur metabolism influenced basal JA levels (Hirai et al, 2003;Maruyama-Nakashita et al, 2003;Nikiforova et al, 2003;Rodríguez et al, 2010).…”

Evidence for a SAL1-PAP Chloroplast Retrograde Pathway That Functions in Drought and High Light Signaling in Arabidopsis

“…Inositol 1,4,5-trisphosphate (IP 3 ) is viewed as one of the most logical targets for SAL1 in vivo (Xiong et al, 2001;Zhang et al, 2011). However, other findings using mutants and transgenic plants suggest SAL1 may be degrading 39-phosphoadenosine 59-phosphosulfate (PAPS) (Rodríguez et al, 2010) or 39-phosphoadenosine 59-phosphate (PAP) (Gy et al, 2007;Kim and von Arnim, 2009). Moreover, the enzymatic activity of recombinant SAL1 is similar for both phosphoadenosines (Gil-Mascarell et al, 1999), but the phosphatase activity against IP 3 is only 4% of that against PAP (Xiong et al, 2001).…”

Plastids Are Major Regulators of Light Signaling in Arabidopsis

“…The oligonucleotides used for qPCR analysis of RbcSA1, PsbS, CHS, and AOS expression were 5#-AATTTCCGGACTTAACGTTTGTTT-3# and 5#-CATCAGACAGTTGAGAATCCGATAGA-3#, 5#-CGGCAAAAACG-TCCGATCCTG-3# and 5#-GTGAACCCAAACAATGGACCTTG-3#, 5#-TCGG-ACCAGGTCTCACTGTTG-3# and 5#-AGGCAAGCGTTCTGTTTAGAGAG-3#, and 5#-GGAGAACTCACGATGGGAGCGATT-3# and 5#-GCGTCGTGGCTTT-CGATAACCAGA-3#, respectively. The oligonucleotides used for qPCR analysis of AAA, BAP1, CCA1, CDKB2.2, FER1, Lhcb1.4, LOX2, MCM5, NodL, PRR5, and ZAT12 expression were described previously (Mockler et al, 2004;Li et al, 2006;Baruah et al, 2009aBaruah et al, , 2009bShultz et al, 2009;Rodríguez et al, 2010;Adhikari et al, 2011;Wang et al, 2011b). We calculated relative mRNA levels using the comparative cycle threshold method (Pfaffl, 2001) or the relative standard curve method according to the manufacturer's recommendations (Applied Biosystems).…”