Enlarged meristems and delayed growth in plp mutants result from lack of CaaX prenyltransferases

Abstract

Meristems require a myriad of intercellular signaling pathways for coordination of cell division within and between functional zones and clonal cell layers. This control of cell division ensures a constant availability of stem cells throughout the life span of the meristem while limiting overproliferation of meristematic cells and maintaining the meristem structure. We have undertaken a genetic screen to identify additional components of meristem signaling pathways. We identified pluripetala (plp) mutants based on their dramatically larger meristems and increased floral organ number. PLURIPETALA encodes the ␣-subunit shared between protein farnesyltransferase and protein geranylgeranyltransferase-I. plp mutants also have altered abscisic acid responses and overall much slower growth rate. plp is epistatic to mutations in the ␤-subunit of farnesyltransferase and shows a synergistic interaction with clavata3 mutants. plp mutants lead to insights into the mechanism of meristem homeostasis and provide a unique in vivo system for studying the functional role of prenylation in eukaryotes.

Protein Geranylgeranyltransferase I Is Involved in Specific Aspects of Abscisic Acid and Auxin Signaling in Arabidopsis

“…This finding implicates protein farnesylation in regulation of meristem size. Similarly, loss-of-function mutations in the Arabidopsis PLP gene, which encodes the shared a-subunit of PFT and PGGT I, cause an enhanced response to ABA, dramatically larger meristems with disruptions in the pattern of cell layers, and flowers with significantly greater numbers of floral organs, especially petals (Running et al, 2004). Together, these observations establish roles for PFT in negative regulation of ABA signaling and meristem size.…”

“…The only reasonable way to discriminate between these possibilities is to examine the phenotypes of mutants lacking PGGT I, but not PFT, activity. The ABA phenotypes of era1 and plp mutants present similar difficulties (Running et al, 2004) and suggest that PGGT I may play a role in ABA signaling distinct from that of PFT. For example, PGGT I may positively regulate ABA signaling.…”

“…However, the phenotype is relatively weak, and many era1 flowers have the normal number of four sepals and four petals (Running et al, 1998;Bonetta et al, 2000). plp flowers, on the other hand, exhibit a much stronger phenotype, averaging 5.1 sepals and 8.7 petals per flower (Running et al, 2004). This result can be interpreted in two ways: either floral organ number is governed by both farnesylated and geranylgeranylated proteins, or floral organ number is governed only by farnesylated proteins and PGGT I partially compensates for loss of PFT activity in era1 flowers by prenylating a subset of PFTsubstrate proteins.…”

“…Three protein prenyltransferases are known to catalyze protein prenylation in plants and other eukaryotes: (1) a heterodimeric protein farnesyltransferase (PFT) that consists of a-and b-subunits and transfers a farnesyl group from farnesyl pyrophosphate (FPP) to proteins bearing a C-terminal CaaX motif, where ''C'' is Cys, ''a'' is often an aliphatic amino acid, and ''X'' is generally Met, Ala, Gln, Ser, or Cys; (2) a heterodimeric type I protein geranylgeranyltransferase (PGGT I) that shares a common a-subunit with PFT but possesses a distinct b-subunit and transfers a geranylgeranyl group from geranylgeranyl pyrophosphate (GGPP) to proteins bearing a C-terminal CaaX motif, where ''X'' is Leu; and (3) a heterotrimeric type II protein geranylgeranyltransferase (PGGT II or Rab PGGT) that consists of distinct a-and b-subunits, as well as a third subunit called the Rab escort protein, and transfers a geranylgeranyl group from GGPP to Rab protein substrates (Clarke, 1992;Zhang and Casey, 1996;Crowell, 2000). PFT subunits have been identified and characterized from pea (Pisum sativum; Yang et al, 1993;Qian et al, 1996), tomato (Lycopersicon esculentum; Yalovsky et al, 1997), and Arabidopsis (Arabidopsis thaliana; Cutler et al, 1996;Pei et al, 1998;Running et al, 2004), and PGGT I subunits have been identified and characterized from Arabidopsis (Caldelari et al, 2001). These and other studies establish the functional similarities between plant, yeast, and animal protein prenyltransferases (Crowell, 2000).…”

Farnesol kinase is involved in farnesol metabolism, ABA signaling and flower development in Arabidopsis

“…Furthermore, ABA-insensitive abi3 mutants have an early-flowering phenotype (Kurup et al, 2000;Rohde et al, 2000a,b). Loss-of-function mutations in the Arabidopsis PLURIPETALA and ENHANCED RESPONSE TO ABA1 genes, which encode the a-and b-subunits of protein farnesyltransferase, respectively, cause an enhanced response to ABA, enlarged meristems, and supernumerary floral organs (Cutler et al, 1996;Pei et al, 1998;Running et al, 1998Running et al, , 2004Bonetta et al, 2000;Yalovsky et al, 2000;Ziegelhoffer et al, 2000). However, to our knowledge, the data shown here are the first to establish a conditional developmental phenotype that links abiotic stress signaling to flower development.…”