{"doi":"10.1105/tpc.001792","title":"Heterotrimeric and Unconventional GTP Binding Proteins in Plant Cell Signaling","abstract":null,"journal":"The Plant Cell","year":2002,"id":656879,"datarank":0.8117469077782561,"base_score":5.4116460518550396,"endowment":5.4116460518550396,"self_citation_contribution":0.8117469077782561,"citation_network_contribution":0.0,"self_endowment_contribution":0.8117469077782561,"citer_contribution":0.0,"corpus_percentile":null,"corpus_rank":null,"citation_count":223,"citer_count":0,"citers_with_citation_signal":0,"citers_with_endowment":0,"datacite_reuse_total":14,"is_dataset":false,"is_dataset_confidence":null,"is_data_producer":false,"deposit_databanks":null,"is_oa":false,"file_count":0,"downloads":0,"has_version_chain":false,"published_date":null,"fair_score":null,"fair_percentile":null,"algorithm_id":"datarank_citation_only_1hop_v6","ranking_scope":"data_only","authors":[{"id":406496,"name":"Sarah M. Assmann","orcid":"0000-0003-4541-1594","position":0,"is_corresponding":false}],"reference_count":0,"raw_metadata":{"has_enrichment":true,"resolved":true,"title":"Heterotrimeric and Unconventional GTP Binding Proteins in Plant Cell Signaling","abstract":"Signal-transducing GTPases in plants include small G proteins, heterotrimeric G proteins, and, potentially, several unique types of GTP binding proteins that are not members of either of the aforementioned classes. This review will focus on recent discoveries concerning the roles of heterotrimeric and “unconventional” G proteins in plant cell signaling. Small G proteins are reviewed elsewhere in this issue (Yang, 2002). Plant heterotrimeric G proteins have been the subject of several other recent reviews to which the reader is also referred (Ma, 1994; Assmann, 1996; Hooley, 1998; Bischoff et al., 1999; Fujisawa et al., 2001). Ma's review (1994) does a particularly good job of summarizing the early, mostly biochemical and immunological, progress toward identifying plant G proteins, which will not be covered here. Mammalian Heterotrimeric G-Protein Cycle. (A) Classic heterotrimeric GTPase cycle. Ligand (L) binding to a GPCR activates the associated G protein, promoting Gα and/or Gβγ interaction with downstream effectors (E). Intrinsic GTPase activity of the Gα subunit eventually returns the G protein to an inactive state. The Gα subunit remains closely associated with the plasma membrane. (B) Certain Gαs (von Zastrow and Mostov, 2001; Zheng et al., 2001) can show dissociation from the plasma membrane upon GPCR activation, contingent upon the absence or removal of lipid modification and the presence of regulatory (R) proteins. Lipid Modifiers and Effectors of G Proteins. (A) Three types of G protein lipid modifications are shown. N-Myristoylation occurs by the attachment of the saturated fatty acid myristate (blue) to a conserved acceptor Gly (red) next to the initiator Met via a stable amino bond. In palmitoylated proteins, the saturated 16-carbon fatty acid palmitate (blue) is attached to Cys residues (red) via a labile thioester bond. Protein prenylation involves the attachment of the 15- and 20-carbon isoprenes farnesyl and geranylgeranyl (blue), respectively, to conserved Cys residues (red) at the C-terminal ends of proteins via a nonreversible thioester bond. The acceptor Cys residues are part of a conserved CaaX box motif in which C indicates Cys, a represents an aliphatic amino acid, and X is usually Ser, Met, Cys, Ala, Gln, or Leu. Ct and Nt indicate C- and N-terminal amino acid positions, respectively, relative to the acceptor amino acid. Proteolysis removes the final three amino acids, and the new C-terminal Cys is then prenylated. The Arabidopsis prototypical GPA1 contains a conserved myristoylation motif and a putative sequence for palmitoylation in the N-terminal region. The two Arabidopsis G protein γ subunits (AGG1 and AGG2) contain a prenyl group binding site in the C-terminal region. (B) Cleavage sites and hydrolysis products of phospholipases regulated by G proteins. PLA2 is an acylhydrolase that specifically removes the acyl chain from the sn-2 position of the glycerol backbone (black). PLD and PI-PLC are phosphodiesterases that generate similar products, except that the phosphate group (blue) either stays with the lipid moiety (black) or goes with the head group (red). DAG, sn-1-palmitoyl,2-linoleoyl diacylglycerol; Ins(1,4,5)P3, inositol 1,4,5-trisphosphate; LysoPtdCho, sn-1-lysophosphatidylcholine; PtdCho, sn-1-palmitoyl,2-linoleoyl phosphatidylcholine; PtdIns(4,5)P2, phosphatidylinositol 4,5-bisphosphate; PtdOH, sn-1-palmitoyl,2-linoleoyl phosphatidate. Mammals also possess ∼5 distinct Gβ and at least 12 Gγ subunits (Seack et al., 1998; Cook et al., 2001). A hallmark of the ∼35-kD Gβ proteins is the WD-40 motif, consisting of seven or eight tandem repeats and a conserved Trp-Asp (WD) motif. These repeats assemble into a seven-bladed β-propeller structure (Lambright et al., 1996; Sondek et al., 1996). Gγ proteins range in mass from 7 to 10 kD and are not highly conserved. However, all Gγs possess the C-terminal CaaX (where “a” is an aliphatic amino acid) site for isoprenylation (Figure 2A), which confers membrane association. A coiled-coil structure formed between Gβ and Gγ results in a noncovalent but very tight interaction between these two subunits, such that they function as a nondissociable dimer. A nonexhaustive list of some Gα subunit effectors in mammalian systems includes adenylate cyclase, cyclic GMP phosphodiesterase, phosphoinositide 3-kinase, the phosphoinositide (PI)-phospholipase Cβ (PI-PLCβ; Figure 2B) (Singer et al., 1997), phospholipase D (PLD; Figure 2B) (Singer et al., 1997), Na+/H+ exchange transporter (Voyno-Yasenetskaya et al., 1994; Voyno-Yasenetskaya, 1998), the TUBBY transcription factor (Santagata et al., 2001), and K+, Ca2+, and, to a lesser extent, Cl− and Na+ channels (Brown and Birnbaumer, 1990; Morris and Malbon, 1999; Reddy et al., 2001). Gβγ targets include phospholipase A2 (PLA2; Figure 2B), calcium channels, and some isoforms of adenylate cyclase and PI-PLCβ (Jelsema and Axelrod, 1987; Logothetis et al., 1987; Kim et al., 1989; Katz et al., 1992; de Waard et al., 1997; Morris and Malbon,  A nonexhaustive list of some  that  with  to  mammalian heterotrimeric G protein  includes   members of the     members of the    and    members of the   and   and      this   is not  that  in G protein   are  for     In  some    G protein   the  from     of   and     of  are        of an   on Gα   GTPase   in  Gα   this  is conserved  all   some types of Gαs   by    of   to  factor     Gα  on a Cys  the Gα C    of  by  with       include   which  G proteins in      which  the inactive  and the    which activates G proteins by  the  of an    et al.,  In  to  and  such as   the Arabidopsis  contains    Gα  GPA1  et al.,  GPA1 is   to  and     the conserved  site for  but contains the sites for  and for   et al.,   sequence    and  Assmann,   also  a  palmitoylation site (Figure   of GPA1 have been  from several  and    Plant G Protein  Plant G Protein  GPA1 is a   in  but some   such as  have been  to have two closely  GPA1   et al.,   et al., 1996).  is also a    from     that is    to GPA1 and   a   of plant Gα   et al.,     of Arabidopsis GPA1  not been    GPA1  been  to   with a  dissociation   et al.,  The  G protein     been  to function as a Gα by  biochemical    for binding  for   other   GTPase  and  by   et al.,  1997;  et al.,  GPA1  and protein are  in all  except    et al.,  and GPA1  is particularly  in   and    such as    and    and    et al.,   et al.,  A similar   been  for     et al.,    is highly  in  and   et al.,   GPA1  been  to the plasma membrane and   in  Arabidopsis and    et al., 1997;  et al.,     been  in  membrane proteins  et al.,  A putative Gα subunit also  been  to the  cell  of the     et al., 1998),        et al.,  or  channels  and  1996). The  of Gα   by    been  in several   not  in  In   the    acid     in     have    acid     and  acid      et al.,   and   also have   on     in   is  by   et al.,     of  by   not been  to  the   does contain an    sequence  et al.,  In   of  which have     from  by     also is   et al.,   with Arabidopsis GPA1  in   In    of     been   et al.,  The Arabidopsis  also contains   Gβ   with   to mammalian Gβ subunits (Ma, 1994;  et al.,  and  have been  in      and    et al., 1994;  et al., 1996;  et al., 1998;  and    et al.,  Arabidopsis and  Gβ  are  in   and    et al.,   of   is  in   in   et al., 1996).    closely  the    for  with the  that       been  to the plasma membrane as  as the   in  with the  of Gα  et al.,  In   Gβ  been  in  plasma membrane and   by protein    and   with    with    Gβ   to lipid   the plasma membrane  et al.,  Lipid  are   of unique lipid  that are  to    proteins,   promoting  association.  mammalian  and  also    to  with lipid    is  in  which are cell   that are  in the protein   and  2001). Gγ   be  on the  of sequence     two Arabidopsis Gγ subunit   and    by  of  interaction with a  Gβ protein in the     and   2001). The  Gγ subunits are   to  other and   to   with  mammalian Gγ   and   possess   Gγ   small   and   a C-terminal CaaX motif, and an N-terminal  with the  structure to  with a Gβ   and  also  with Arabidopsis  in    and in  binding   and   2001).  and   are  in all  with an   for the  part  to that of   and   2001).     G proteins in       to     with   membrane  and GTP hydrolysis by   as  be     a G protein   et al.,    not   of a  for GPA1 in   recent  are  with such a  These   two    of GPA1 and     et al., 2001). The        but show  cell  in   and    from the  of the    in the   are  of  of the   of the cell  cycle. The   of GPA1   in   is  with a  for GPA1 in cell    with this  is the  that    that  GPA1 progress    the cell   et al., 2001).  the  of  Gα subunits in  also  cell   of that   and   and this occurs  a   of       cell  via an  G    the  of Gα in  cell    from an interaction with downstream proteins that  a conserved    downstream  is  a  G protein  in mammalian systems that  cell  in   not  cell types  and  2001). PLA2 is  by  in  cell   and  1989;   and       the cell  in  plant   and      also  an  in   to a     The   is  in a   that  be  in    et al.,   et   a   to  in the       that GPA1 also   a  in   and signaling.  the Gβ     a     et al., 2001),  that a  G protein   be  in the  of   In  the     in   similar to   by the       with   and       In  with the  that G    in the   of plant  heterotrimeric G proteins have been  in  acid   in    in   of the  of  in   have  from   The     to a G protein  subunit   as  by    several    and by     plants  the    et al., 1999; Fujisawa et al.,  which includes not   plant  as a  of    but also      and    of  and    et al.,  In the   of    an   in   by the   of   such as  that   the    that  the  of the   The      as    on the  that      not  in    et al.,  In           of the    and of the  transcription factor  to  this   et al.,  Fujisawa et al., 2001).  with this          that  and    of an     and        by   et al.,  These  also  that Gα and the   Gβ   are  in the     A    in this   also   a Gβ    sequence  with   is not as   et al.,  In  to  the  of  small or heterotrimeric G proteins  et al.,  also          in     and    the   G protein  in   in  the Gα subunit does not   for this  in        can  the  of   of     as  as   of    et al.,  In  and at    G protein  also  to  a  in  the    by   of the  downstream effectors of the   is  which   acid and a head group from   (Figure 2B)  and   In    PLD activity in    and  and    the   of this   also  the   of     and     at the   of a heterotrimeric G protein  in this  is   such a   be  with other  that have    for G protein  of PLD in the   of   and in PLD  in    et al.,      GPA1    PLD in biochemical  of PLD activity  and  2001). This  is    is  with  and the   that  G protein   the  of   from the membrane. PLD also is  by  in     et al.,     not   a  interaction of Gα and PLD in this     that    G proteins in this cell  as    the      by  et   that   of    is  in these   et al., 2001).    of the   channels that       also is  However, not all  cell   are    of   is  In    from the     of  channels that   and Cl−     occurs     is  to  but is     is   These results  that a  of      on   in      in   or as a   a      This  of    by a G protein is   that  a  mammalian  channels have been  to be regulated by G proteins  et al., 2001). The results with the   are  with an   of G protein  of plant  channels, in which    that   and     channels of         activity  and Assmann,   and   The  of    by    to    that     GPA1 to       et al.,  have  that  activates  in   which  inositol  and  (Figure  the     from     and     the   channels  and   In mammalian  G proteins function  of the  of   will be  to     of  cell  is  in the    with this  In     to         not   and PLD but also cyclic  and     et al.,   and  2001;  et al., 2001).  of these  by GPA1    also have  the  of    activity by   and  and the  by  in   of  cell plasma membrane  and Assmann,  in  in which the     of the  membrane   by the    not   in   to  in this    channels  with the  channels and are  by  to  a    of   in the  of the    this   is  that  activates  cell  channels in  membrane   et al.,   is  that GPA1     to  the    either by   interaction with the  or   proteins or    This  is   by the  that  can    channels   in  membrane  a similar   to be  for the    The presence of   and      indicate the  of a   of the  cell  to  and   also is some    with a  for G protein  in     et al.,   et al.,   and    these  have  to be  by   a  for  G proteins  on the   is     in mammalian   and   in  to  adenylate  However, the  of plant G protein  subunits  that this     in plants either from  via an  G protein   or from    of the   of the   that   the  of G protein      been  that    on   to generate     on the  of     et al.,   that  cell  can  in     in the   is  for G protein  in      also  G proteins in    in other types of plant    and       in          and      and Assmann,  In   of this        et al.,  which is an   to that  with  and   will be  to   this    that of the    of   is  in    In     of the   subunit     as does the  of    However,  of     the   a  in    These   results  the  to   protein  in   an  that the       et al.,   and de   have    to  a G protein in a   of  of two   channels in    of which    and the other of which        is  of the   in which heterotrimeric G protein    in  A  biochemical  by  and   that a   of       GTPase activity in  plasma   from   of   The  G protein is  to be a   protein that  a GTP  in a   is  by   and is  by  and   et al.,    in    two G protein  subunit   and   which of these is  by   remains to be   similar  G protein  of    by  in a    also  been   et al.,    have  G proteins in   and    by     that the  of  into the  of    by      by    the  of    of   to  or    et al.,   and    of       binding by plant  and the      by    et al.,   which activates G proteins,     in    and  cell   et al.,   and    the  of   on these   and   et al.,   et al.,    cell   and   to    the  of heterotrimeric G proteins in     the  A     to   G protein          and    a     of    into      to   these  in a cell  and     of either  or  with   the    of         as  downstream of the G    to this  is the    or  of   the    The  to which this     the  of  a cell   or   is not    group  Arabidopsis with   of a    either GPA1 or this   to  a   Gα  et al., 2001).   that Gα   to  of    by   and   but does not   to     is   for    and in a     the  to    by GPA1  is           of   and GPA1  of      not   the GPA1    into a   However, the  of GPA1       in a    that  is not a   for this    These results  that  GPA1     at  with the results of  et     that   plants also  a      et   from   that GPA1   cell  and not cell    et   that   GPA1    by  cell    cell    as  et   is that the   of GPA1   upon this protein a function that  does not   in       of  of some mammalian Gαs  to an    of the subunit      to  these  is to  that   GPA1 or  GPA1       in an  of  Gβγ subunits, and   is these  Gβγ subunits that  the   However, this  does not  the  that  group  an  on cell  and the other group  an  on cell     of either cell  or cell   been  in  plant  and    et al.,  and     of the      is  for the     G proteins  to be   of   in plant    et al.,   and  1997;  et al., 1997;  1998;  et al., 1998;  et al.,    is  for the  of plant heterotrimeric G proteins in  to   and     et   that stable  of  plants with the  subunit of   in   to    of  acid, and   of   A  of plant G proteins in plant  to     by the  of  et     that   an   in  cell     the   by the       that the   acid and the G protein      activity in this   to an  in inositol   et al.,   group   in  that   from the     membrane    to    activity and   in  plasma membrane   also  plasma membrane    or     these        et al.,     by  occurs  with a  in the    and  and    as    also  from a   a  protein that  with Gα   biochemical  for   of a G protein  et al.,  In   group      that a    of  GPA1  the activity of a   that they  is  in   in  calcium  et al.,   also can  the  of plant    et   that    the  of   in   of     and   a phospholipase  and PLA2 products such as  and  acid    in  to      have been  to  heterotrimeric G proteins in    to     which    in   is a    is  by      of an       but    by    also     in     et al., 2001),  by  the    et al.,  and biochemical   that   and  factor  PLD and  activity   et al., 2001). G proteins also have been  in the  of    the    et al.,      in this        as does  of  A  plasma membrane protein from   can be  by    conserved  of mammalian Gα subunits and can     plasma membrane  contain a GTPase activity that is  by   will be  to     Arabidopsis    the  G protein  and the  of   in that    been  as an    in  the   and     factor      et al.,  and  stable  in  calcium  et al., 1997),          have   and  as  downstream of  in the  of   in the    et al.,    does not    in    et al.,  but the  that G proteins      not been      been  concerning the  of G protein  on   in   However,  et    that a heterotrimeric G protein      to    the   is  that G proteins     as  as      et al., 1990;  et al.,   and    et al.,  The GPA1 subunit  to  the plasma membrane and the     is  in   These  sites of G protein      of plant  Heterotrimeric G protein subunits, and   have been  to the  in mammalian  in which  in cell   protein   and   and   have been      and    least  mammalian Gα subunit also  been  to the       to    in protein   et al.,    include the  the   and the    in   and   have been   et al.,     Zastrow and Mostov, 2001; Zheng et al., 2001).   the  of prototypical  in the Arabidopsis    the  of GPA1 and   the   and  are    have several  of “unconventional” GTP binding proteins    have   to be   group of  G proteins is the  G  which in Arabidopsis  three    and   and Gα putative show  and   to  at the amino acid      is  similar to   to     been   and Assmann,   is   the plant and  a  protein with a C-terminal     with Gα proteins,    for GTP binding as  as an   and a     of Gαs as  to small G proteins.   protein  GTP   other   the  of the  protein    to   GTPase activity   and  Assmann,    is  that       some of the conserved amino   from  on mammalian systems to be  for GTP   is  that the  structure of the protein   for the  of these  A unique  of  is  N-terminal  which contains a   that is similar to    and a   The  box is a  sequence  in proteins of the   membrane  in the  of  such as   and    of the presence of  in the    this membrane    an   to    The  box  with  proteins in the    and this interaction is  to    to the  membrane for  in      et al.,   the  box of   an      The  box is not  in the other members of this   and to    have not been   the plant   are  identifying    of the   to   associated with      and  Assmann,     protein in Arabidopsis with  GTP binding  is      of the    that   an  protein with two  that are conserved in GTP binding proteins  et al.,    are        on the  of   and     with     and   However,    et al.,   that the  protein is  for cell  in  as  as  with  cell  in the      of    a   similar to that  in  Arabidopsis  with   of GPA1 protein  et al., 2001;  et al., 2001).   of  GTP binding proteins  in plants is the  regulated G proteins  Plant  are  in all  at the  and protein  with   of  and protein  in    such as   and    et al., 1999;  et al.,  The  of  and Arabidopsis    to be regulated by the cell   et al.,  and Arabidopsis  protein  been  to     et    that    a  in   The    of this  of G proteins is   sequence  which   and    2001).    is   to  members of this  The    of   a  and  function for this  of GTP binding proteins  and     G proteins also are   Arabidopsis   et al.,  and   at the    et al.,     in a  for    that      small       of  to Gαs and to the   The function of  remains     as a    that     and  1996).  the   from a   is  into a   a  in     the   for the       a  with  sequence  with  protein of  function  et al.,  However,        an  structure for  similar to that of Gα   is   kD  and   of  with     at   the  of  in the  and  et   that the  protein     by  cell  a  similar to that  by  mammalian small G proteins as  as Arabidopsis       have been  to  in   et al.,   1997;  and    have three  and three      are  and  C  are  (Figure    the  members of a     of proteins, the   exchange   which  the exchange of GTP for  on the G protein    of Mammalian    Heterotrimeric G Protein    of Mammalian    Heterotrimeric G Protein    as for   and  the  of mammalian    to be a   of the  of this  of proteins in   are three   as putative  in  of        with   and  1997;  et al., 1998;    is  with the      and  1997;  et al.,   the      to   with the   also is  to have an    and a  C  as  for  and   of several  amino acid residues as  as an    site that is  in    is  at a   in   and   et al.,      to be  in      plants  a    et al., 1998), but recent  indicates that the      by an    and  2001;  et al., 2001).  the   of  remains    the   of mammalian       show   to   in the   which are the  highly conserved  of these proteins  et al., 1994;  and    the  remains that  not   as  will be  to  this  in    of  is the  which possess   sequence  to mammalian  but have been   to have a    et al.,   are  to be    in Arabidopsis  et al.,  a  in  with the    of G protein  in this  The    is  to   and     of  a G protein is  to be  in this   other members of the      to be G protein   the  of GPCR  in mammalian  and in the  recent results have  that not all mammalian heterotrimeric G proteins   for    not all    with heterotrimeric G proteins  et al., 1999;   In a    in  three  mammalian proteins,  to    of G protein    to  G protein   et al., 2001)    is a  protein     to function as a   GTP binding to  In  the proteins   closely to  are  in the   of small G proteins (Yang, 2002).  is a   of the  protein  and  with Gβγ  Reddy and   that the Arabidopsis    that have  with     is a   protein that  the dissociation of  from some  this  with GTP binding to Gα and    et al.,     as a  dissociation   a  of regulatory proteins    for small G proteins   et al.,   et al.,   et al.,   the   of    Gα   these   the   that   with Gβγ for binding to Gαs  et al., 2001),   for        for the   of  The Arabidopsis    which  as a   of     to    et al., 1996;  et al., 2001), is a protein with 10  repeats  et al., 1996;  et al., 2001) and   sequence  with      by  a G protein  of the   Mammalian G protein   are regulated  at the  of the   and at the  of the    of regulatory proteins are  in    is an   of  at the    protein  A and   of which can be  by  protein    and     to the G protein, a   as     is  by GPCR   that           which are  proteins, to the    et al., 1999; Morris and Malbon, 1999;  2001;  and  2001).  the  of the    of Gβγ  a       2001).    that have  sequence  with mammalian  are  by the Arabidopsis   to      and the    of      which  to   the   G protein regulatory   in    binding to and  the  of    the  at which Gα  GTP by as  as   and    the  of  this  to the  of G protein signaling.        GPCR  is  but   the  of the G protein   in the presence of an   This     but  can   the   exchange   by   to  the  the G protein, and the   such that not   but also  occurs at a     can    of the G protein by  as  proteins that  the  G protein, and  in a stable   that is   in the absence of     et al.,   and     in    are   types of mammalian  proteins,    proteins, and  Arabidopsis   PI-PLC  but these     of the   an   with  but  the  C-terminal regulatory  that is associated with  activity in   is particularly  that the Arabidopsis   not to    proteins    et al., 2002).  proteins  a   of  members in   and  1999; Zheng et al., 1999; de  et al.,   and   and  G proteins via   activity and, in some  via  with downstream effectors for binding to Gα  et al.,   is    for  plant sequence  of   1998;  et al., 1998;  et al., 1998),  on     However, the  of   is not  to  the  that   proteins  be  in    mammalian  and  have  sequence   at the protein   an      that these proteins have  of   that can  for the  that these  proteins  possess  activity  et al.,   new types of    in plants that   or  sequence  with mammalian    can be palmitoylated  and  1996). This lipid modification  of the attachment of palmitate  via a thioester  and occurs at a conserved Cys  in the C-terminal   Heterotrimeric G protein  and γ subunits also are subject to lipid modification (Figure    of the  attachment of myristate  to an N-terminal Gly  in Gα via the  bond.  of Gα    palmitoylation at a Cys   the   and  interaction with   three of these   Gα  to the plasma membrane  1994;  et al., 1999;  and  2001).  on the   these lipid modifications also  be  for   by regulatory proteins  et al.,   is   this lipid modification as a  by which Gα  and activity  be   and  2001; Zheng et al., 2001).   in Figure  GPA1   myristoylation and  palmitoylation   is  by    This    to be  at the biochemical  in  but several plant proteins contain myristoylation sites  et al., 1999;  et al.,  and   have  that  of the myristoylation site in the  protein, which  in    plants  to    et al.,  In  palmitoylation  been   for the   protein  and   These  have    on G protein  but are   they  that plants possess   and  acyl  that   GPA1 as a  Gγ subunits are subject to  either   of a   or   of a 20-carbon  Gβ  with Gγ occurs in the  and prenylation occurs  to this   and  1996).  is  for   with Gα and  membrane association. In  prenylation  been  as  to  with Gβγ  for  Gβγ  of   prenylation  and  1996).   in Figure   and  contain the conserved CaaX sequence for   is  by farnesyl   and    and    or   geranylgeranyl   and   a   subunit and have distinct  subunits  et al.,    for all three of these  have been  in plants  et al.,   et al., 1996;  et al., 1996;  et al.,   for  have been  in  and   et al., 1996;  et al., 2001). A  for the  subunit    from Arabidopsis  et al., 2001). The  subunit    from   et al.,  and an Arabidopsis      to    by    et al., 1996).  is the  subunits that    and   have been associated with    and  in    to  in   and    et al., 1996;  et al.,  The     been   and  to    and   and several    et al.,   the roles  to heterotrimeric G protein  in   and cell    be of   to  the prenylation   and  of  and  in the    A     the mammalian  is the  that the Arabidopsis     prototypical Gα   prototypical Gβ  and two   Gγ   is  that  this  of G proteins,   of GPA1 and  are not   least  the   to  these    to   but not to  plant  or   proteins, which  be  by     roles in  that   of  The  of  and   is     the  of  in which GPA1 and  have been    and     and  and     of the Arabidopsis   is  by a  range of G protein  of which     as    these  be the  that  G proteins to       Arabidopsis       to   that   of G protein   to be    is that  of the   heterotrimeric G proteins in a      the  of plant   and   on       to   plant Gαs  not  to contain the conserved     is  that  targets  site on the plant  for   of the two   Gα subunits contains a   site  and     et     of a  protein that  with Gα      G   elsewhere in the   chain  at the Gα  or     protein  in which   is not a    for heterotrimeric G protein  in   this     then the  of  in which heterotrimeric G proteins have been   be   is  at     to be a   not   in plant G protein   been  in G   not  in  and    but also in  cell  to    and  by    of   and     via  and/or PLD also  been  in several  to  downstream of plant heterotrimeric G proteins.  via PLD is of      not  mammalian PLD regulatory   via small   heterotrimeric G proteins.     the   of G protein     et     of   in        is  in  the   of the  The    from  associated with the Gα C  which is  in  and Arabidopsis  et al.,   of the Arabidopsis and      for the  of   proteins that  plant heterotrimeric G proteins and will  a   for  the  to which plant G proteins have  distinct roles in          for the  of       for  on    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