Year: 2002
Type: review
Abstract: The power of molecular genetics has dramatically advanced our understanding of all aspects of gibberellin (GA) signaling. Many genes encoding GA response pathway components have been identified using Arabidopsis and cereal mutants, and more elaborate genetic screens are producing additional mutants that are providing new insights into this pathway. Now, a confluence of new approaches, such as functional genomics and proteomics, promises even more rapid progress in unraveling the physiology and biochemistry of GA-regulated processes. New levels of regulation are being identified that indicate that the GA response pathway is linked tightly to its biosynthesis and catabolism. Furthermore, the GA metabolism and response pathways integrate with other signaling pathways to regulate plant growth and development, and the interaction between these response pathways is likely to be extremely complex. Several recent reviews have described GA biosynthesis and catabolism (Lange, 1998; Kamiya and García-Martínez, 1999; Hedden and Phillips, 2000; Yamaguchi and Kamiya, 2000) and the GA response pathway (Thornton et al., 1999b; Lovegrove and Hooley, 2000; Sun, 2000; Richards et al., 2001). This review focuses on recent results in the field of GA signaling. We begin by considering the aspects of the homeostatic and developmental control of GA biosynthesis and catabolism that relate to signaling. Then, we discuss components of the GA response pathway that have been identified primarily through the analysis of mutants exhibiting altered GA responses. We conclude with a summary of the cereal aleurone, which has proven to be an excellent model system for studies of GA signaling. GAs form a large family of diterpenoid compounds, some of which are bioactive growth regulators, that control such diverse developmental processes as seed germination, stem elongation, leaf expansion, trichome development, and flower and fruit development (Davies, 1995). There is much evidence that environmental stimuli, including light and temperature, can affect plant processes by either changing the GA concentrations and/or altering the responsiveness to GA (reviewed by Davies, 1995; Kamiya and García-Martínez, 1999). Major GA Biosynthetic and Catabolic Pathways in Higher Plants. The enzyme names are shown in boldface below or to the right of each arrow. GA9 and GA20 also can be converted to GA51 and GA29 by GA2ox. GA4 and GA1 are the bioactive GAs, and GA34 and GA8 are their inactive catabolites. The biosynthesis of GA in higher plants can be divided into three stages: (1) biosynthesis of ent-kaurene in proplastids; (2) conversion of ent-kaurene to GA12 via microsomal cytochrome P450 monooxygenases; and (3) formation of C20- and C19-GAs in the cytoplasm (Figure 1). In the first stage, geranylgeranyl diphosphate, which serves as a common precursor for diterpenes (e.g., GAs and the phytol chain of chlorophyll) and tetraterpenes (carotenoids), is synthesized by either a mevalonate-dependent or a nonmevalonate pathway (reviewed by Lange, 1998; Hedden and Phillips, is converted to ent-kaurene in a and by and ent-kaurene with as the In the of the by by ent-kaurene and which can be converted to by In the of GA GA12 and are converted to GA and bioactive GAs, including GA1 and by a of by GA and GA 1). GAs have been identified in higher and a are (e.g., and and Phillips, Many of the other GAs are or of bioactive the pathways in plants that to the formation of GA1 and The of bioactive GAs can be by the of their and the conversion to inactive by which is by GA 1). The of the first in the GA is by and In extremely of are plant development, and the of this is et al., including and higher of The of is to that of the of is much higher that of et al., Yamaguchi and Sun, that the of ent-kaurene is primarily by the and of The of of the and the of the that as a the and of the of GA and each is by a in plant and their is regulation by the of the GA response pathway (reviewed by Hedden and Phillips, genes are in and are in all et al., In the and each is by a and each also (reviewed by Hedden and Phillips, of these genes in plants in some the concentrations of bioactive that the regulation of these genes is in in the of the pathway (reviewed by Hedden and Phillips, 2000; Yamaguchi and Kamiya, of regulation of the GA pathway in the of the pathway (Figure 1). studies that ent-kaurene is synthesized in the and are in this and Kamiya, et al., is a cytochrome P450 enzyme that is to with the (reviewed by and is the ent-kaurene is to the studies of and in that and are to the and are with the et al., In using that is into the the P450 enzyme is on the of the new a for to its these studies the of to the in and some also in the cytoplasm in the of et al., these to in the plants the likely of the the to be is on the in of the of GA in GA response mutants indicate that the of responsiveness to the bioactive GAs GA metabolism by a (reviewed by and 1998; Phillips, 1998; Hedden and Phillips, the of the and the and in the formation of bioactive GAs and are by GA (reviewed by Hedden and Phillips, 2000; Yamaguchi and Kamiya, In the genes encoding which GAs to inactive are by GA et al., 1999; et al., 2001). This regulation the of GAs is in more In the a large of genes encoding in all of the GA and for have been studies with these genes using the of in and genes are to the of GA studies also are the by which the of bioactive GAs are in to regulate plant growth and germination, GA growth and/or the by the and that In Arabidopsis the of GA to be to the of the seed the seed to et al., et al., In and GA has been in the of that the and et al., that affect biosynthesis or seed in Arabidopsis or to the of GA biosynthesis mutants, that GA is to the of the seed and on seed and and In the of and in the and of of Arabidopsis that the of bioactive GAs ent-kaurene in these et al., 2001). in the begin to the of bioactive GA to in which are likely to be the and in the in the control by the GA response pathway. that be for the to the higher of bioactive GA to by Yamaguchi et that the of and to be that of the GA an in in the and in and and in the and in described is a of in the GA pathway in Arabidopsis that the of GAs in the of a pathway or studies evidence that and form a in the et al., that ent-kaurene is the et al., 2001). analysis of in seed be to the of the The of the and of GA biosynthesis seed be of the that the of bioactive GAs by the of between this be the of this pathway. of the of the of GA biosynthesis developmental be to of the and of the pathway as described shown to be to the in leaf et al., ent-kaurene has to be between by the of for the of This be to between the and the studies are to these germination, bioactive GAs stem elongation, leaf expansion, and growth (Davies, 1995; et al., 2001). In the plant bioactive GAs or are in such as the and and seed and et al., 1995; et al., chain or that in and to higher in with et al., et al., 1998; Yamaguchi et al., of using a that is in including and also in the of and et al., In the of Arabidopsis is in the to and in the below the that is elongation, and et al., is in the with the of to be in the below the In the the is in the results for GA in the the and the the studies of the of the and genes in et al., 1999; et al., and et al., this In that in the and in the leaf and the in the of the et al., 1999; et al., In a of in in the a in the of leaf and the et al., The of the much in the that GA is synthesized in the below the and in and that the of be to control the GA in the by GAs synthesized in studies evidence that the genes are in GA biosynthesis in the by the of the genes et al., 1998; et al., of the genes are in the are in the (reviewed by et al., on the of mutants and these genes in the of the of the of genes or in in and leaf which by GA et al., 1998; et al., GA and analysis that the of GA1 and in plants with in the et al., In and evidence that the to a and the first of a et al., In to the of the in the of the the in the and leaf a et that the of the in the of the and that of the in the first of the the of results that the of in the of the in GA biosynthesis to the of the the other GA the of the and the of Arabidopsis flower development, GA is for the development of and and The is in and in et al., also is in the and of the of the genes in and are in the and of et al., 2001). In to in the GA synthesized in the to control the development of other In of the growth and the of and The of with GA to In affect GA biosynthesis et al., 2001). that are in response or in biosynthesis have of the and is by and GA to have on the of this the of on is of GA of by in the which is in GA and The of in GA biosynthesis is by the that the GA1 in of and by the of an or 1998; and 2001). This in the of GA1 in by in et al., The of to stem to the of and the that the to the stem is to the of and to the bioactive GA1 et al., In to developmental the genes of GA biosynthesis and catabolism are to control by light and that also germination, stem elongation, and/or of (reviewed by Davies, 1995; Kamiya and García-Martínez, 1999). of the and control of GA is to the of light and on GA and catabolism genes are or an of in the GA response pathway. is that light seed by GA biosynthesis (reviewed by Kamiya and García-Martínez, 1999; Yamaguchi and Kamiya, 2000) and by responsiveness to GA and plants such as Arabidopsis and light for germination, and that GA the seed response to light GAs the of light in seed and In the biosynthesis of GAs and et al., and light (reviewed by are for seed light to the of that to the of the and that light the GA responsiveness of the In a light the of the bioactive GA1 its and and a light the of the light et al., et that the of bioactive GA4 its precursor in Arabidopsis seed with light higher the in results that of GA is by that the of and in seed of Arabidopsis and in seed of a light et al., et al., The light of of these genes by a light that these genes are by in Arabidopsis and results also that bioactive GA by the of genes seed also the of stem The mutants in and Arabidopsis responsiveness to the bioactive GAs et al., 1995; et al., 1995; et al., results that the of stem by light is with a in responsiveness to light also a in the bioactive GA in the stem is (reviewed by Kamiya and García-Martínez, 1999). Several recent studies in have evidence that of the of GA1 in the of light the of the inactive of GA1 et al., 1999; and García-Martínez, et that the the of GA1 of of the results studies be to GA that and/or the of of using a more et that rapid to of and of are with the of GA1 by or light the of the first to of as a of et that the in GA1 by or light is by the of light is by an light results that the of stem growth by light is by and to the GA1 the of light on stem is in by the responsiveness to in Arabidopsis is by pathways and pathway Arabidopsis is this pathway is of by the pathway. The et al., that GA is for the of by the pathway in The of GA in flower formation in a large of plants also has been by in plants with GA 1995). is to the bioactive GAs that control flower in the of some GAs in the of the of using et al., This identified as of the in this its in the of is the is a of the or of of this the In the of GA1 and GA4 with the of these GAs in stem in et al., et al., described the is in the and in the a for GA in the of the and in the of the the et al., be to the of in the or the the to the the of GA biosynthesis genes to be in is by and by GA (reviewed by 1999; Kamiya and García-Martínez, 1999). plants to form using and plants that is in the and/or of an to the in et al., GA is to have an on recent studies the of light on GA biosynthesis and et al., 2000; et al., genes all of in and in et al., 1999). of the control of either a or the in in and in et al., of in plants the in and altered et al., in the of GA20 and GA1 in the and first of the that of to GA in the and in to is for the light regulation of or GA mutants to form in as as analysis that all three genes in or et al., 1999). concentrations in of plants higher in plants et al., This the that the more stem of plants is by an in GA1 in the with the these results to the that GA is of the in the of is that the of the to the analysis of the of light on GA and the of genes in GA metabolism in and be to the of light regulation of GA metabolism in with in GA in plant we on the insights into the GA response pathway that have the analysis of the genes in these is the in encoding a et al., 1999; et al., 1999). The of GA including and of has levels of of to GA in the the of the leaf to GA that in the the of growth by a of GA in mutants between and a that a of GA response of et al., some of plants are with a in the GA response the of the leaf to GA that these be in all GA responses. in the of In to the results Arabidopsis affect signaling the that is of mutants with GA et al., et al., 2001). the of the in GA between of and a which is a and the which in and to with a that is all family The is in some of the et al., 1999; et al., 1999; et al., and other family are likely to as The of the is for the of these by the GA the which is to with other and the which with is a that identified by its to the of Arabidopsis have been shown to for in et al., 2001). of these is in the of by of in the the of and is by of the is by and a has been shown to GA responsiveness and to the of to and are in seed and also in GA other GA regulation of Arabidopsis a in the and of et al., The Arabidopsis to have and with GA this and et al., et al., is in and GA the of a that is by the et al., of the and of with genetic screens for components of the GA response pathway is that mutants in these components of GA biosynthesis mutants, is by that or et al., et al., The is to the and is to in the of a that the of for mutants that on has identified new GA biosynthesis mutants and et al., plants are that are by the of In the of the seed The of Arabidopsis that are the of and of the of mutants that is in GA et al., 1999). mutants are that have of to and a that affect the GA response pathway. to the mutants, the of plants is In to the described plants also that has a with GA responses. in germination, the being the of and the of genes in the of the et al., of these is that are and with GA biosynthesis the of the with GA the also to in by in with the or the formation of and in in the of et al., In with the formation of et al., 1999). the of in GA is some into is by studies of are of a large with that et al., 1998; et al., be by an the genes that are in a or an in GA responses. mutants of exhibiting in identified et al., 2001). of the leaf and the of in response to with In in the has been and the has to of the which and the of has been of mutants et al., that of a of the family of of GA signaling with of an in response to GA in plants to GA in et al., 2001). Many of the that GA affect genes encoding of the The family is a of the family et al., 1999). In to a of with all of the the of all the which is other et al., et al., (Figure GA are of and are to and and identified in a for the of the et al., of the of including trichome of the of the of the and In to a and Sun, et al., is a interaction between and and Sun, et al., In and the and of even producing a that and are these processes. mutants and in and development, that the are in these processes. shown to be in and Arabidopsis in which the of is to the of by the GA biosynthesis The of Arabidopsis identified as a that GA responsiveness development et al., The of bioactive GAs, that are in the regulation of GA biosynthesis et al., The has a that the the et al., to family and et al., et al., et al., The to the that the Several recent have that is to plants by with a in the of mutants of and in Arabidopsis and et al., et al., 2001). In of the Arabidopsis in and GA of in the et al., et al., that in common to including and (Figure that to have functional Arabidopsis and have been shown to be to the et al., et al., 2000; et al., analysis of that the in and also that the is for the of the GA response pathway et al., The and of that are regulators, and has been to affect is in et al., of the of these also has identified that the et al., Richards et al., is that GA signaling the of the and that the and are for this GA the of and by et al., et al., et al., of the the of and by to by GA et al., et al., The molecular by which GA the of the is is to be et al., et al., et al., The model in which GA the of by their that their GA responses. Arabidopsis in and the of by GA et al., 2001). a GA biosynthesis the of Arabidopsis seed germination, for mutants that the and the of have identified of and et al., for of and also have identified additional and 1995; et al., in the all of the of GA that have been are by and and 1995; et al., 1998; et al., et al., et al., 2001). In a that are the with including more with a and seed and of Arabidopsis in Arabidopsis et al., and et al., the control of the of with GA on these is to be a of the GA response pathway. This is by in which is in et al., the of Arabidopsis using a et al., and by chain et al., have that are all of development and that their is by other or Arabidopsis is in the and the et al., The has with and 2000) and has been shown to have (Thornton et al., is a and enzyme that to and/or of and and 2000; et al., 2001). of is a that and 2000; et al., 2001). The of on and and the by and with other a of and have been shown to be the and these which are can as three the the and the each with a The that are the of have been have been to be et al., 1998; et al., The first of of and the is likely to be the (Figure as for the of et al., 1995; et al., 1998; and that is of a complex. of the the control of the of in Arabidopsis et al., and et al., a The with either by with the formation of the or by with a and the interaction of this with is a and of the converted to a and 1999). The has been shown to with et al., that also is a with is likely that the with additional and that these a in the GA a and of the results in et al., that of is In to Arabidopsis has genes encoding Arabidopsis mutants the have of and the and and that is and that and the have the that is is that mutants that are by in GA response et al., 2001). that has a in light signaling mutants a is to that in the light and of by an a that is by GA and that the of GAs et al., 1999). The is in that are rapid growth et al., that growth in response to is in that are rapid expansion, the of the is likely to of in the GA of et al., that of can regulate GA in a an in GA response or with GA a et al., is of a family with the that be to the can be have a which is to in or regulation 2000; et al., The is a that is to family the of this has been of the and GA and et al., by with a to The to In the of the plants are of the of the be either a or a of GA as a that is a of GA as a that is a of the GA response pathway. a for mutants exhibiting altered of a that is by the described et al., 2001). 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This between the of the GA response pathway and GA in with the rapid of by the GA the plant to GA-regulated processes. GA to in of studies have in GAs in cereal and et al., evidence that the in GAs is for recent has shown that the in GA in the of that GA be in the et al., is that the of GAs is for the of in the et al., The and the are the of GA in as by ent-kaurene in et al., the to in of of and This is by a in GA1 in the of which is to of synthesized GA1 the has been in components of the GA response pathway to the of response genes such as the has been is evidence on studies and and with with GA that the GA in is with the et al., of the GA response also is likely to be with the The of in the GA response in has been by with a of by et al., the which is in the of the et al., 1999; et al., have to GA with the et al., the of the by GA that be and response pathways to analysis that the is to the of et al., 2001). the of which to GA is to and has to GA in and 1999). is to the a In to such as such as and as of GA response in cereal et al., et al., et al., et al., in and in in genes in in In mutants with in the in and in to and in the of GA and more GA the to the of these genes and et al., et al., et al., et al., has been in understanding GA response the of in in is to of with GA et al., This is to the in which rapid of in response to GA et al., 2001). is to the GA response for via the and of the of in response to GA et al., The GA of can be by to The has a the that results in a that also is to The between and the of a that et al., evidence that can as a of a et al., 2000) the in is to this model in an between and response in in response to GA with in in et al., et al., with an of that the in for and et al., There also is evidence that a in the GA response in of in in et al., evidence that a be a for in GA response have been identified in the of genes and et al., and have shown that in these GA response a in the GA of The of the to a GA that the can as a GA response et al., of these a of GA responsiveness in providing functional for their in and and The to as a GA response in of other genes that are in et al., 1999). studies have identified a of GA response genes that are genes et al., 1995; et al., in in to GA et al., In and have shown that to the of the GA response and is to and a of other in in the of GA et al., 1999; et al., 1999). results indicate that an in the of GA-regulated is that the GA regulation of and to GA in with et al., 2001). This is with evidence that GA a in the of of et al., The of of in GA the control of of genes et al., has been identified as a of of an by a is in in the of is to that of by is for is a of et al., This to a the is evidence for GA control of its with other GA in in and et al., and et al., the of signaling in in the GA for signaling is an which for the and of such as et al., and that is by and is a in the and This is to be with the Many GA in cereal are by has shown these signaling pathways in to regulate in the by that signaling of in et al., 2001). This is with the of to et al., and that in by GA et al., et al., is likely to a in the of et al., 2001). is that the GA response between and There is evidence that signaling also be a for signaling. The in is by et al., of GA The and of the GA response components in this review are of for these components also is the the components in a is evidence that this some aspects of the response such as the regulation of GA in all GA to an as GA or
Source: The Plant Cell
DOI: 10.1105/tpc.010476
Authors: Neil Olszewski, Tai-ping Sun, Frank Gubler
Language: English
Subfield: Plant Science
Domain: Life Sciences
SDG: Zero hunger
Open Access status: bronze
OpenAlex ID: W2118433890