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Gibberellins in Pea: From Mendel to Molecular Physiology
John J. Ross, School of Plant Science, University of Tasmania, Launceston, Australia
Early Days of Pea GA Research: The Mutants
The gibberellins (GAs) are a class of plant hormones that affect several important plant processes, including stem elongation, seed development, and seed germination. The effect of certain GAs on stem elongation is especially dramatic, and we have focussed on this aspect in our GA research at the University of Tasmania. We began our studies with a strong emphasis on genetic mutants of the garden pea, especially those with reduced shoot height. One of these mutants was a dwarf variety used by the "father" of genetics, Gregor Mendel (Mendel 1866), which is typically only about one-third the height of tall (wild type) plants. The contrast between dwarf and tall plants was one of the seven distinct differences studied by Mendel. The mutant allele that confers this dwarf habit is now known as le-1, and the normal allele, which confers the tall habit, is termed LE. An early breakthrough in the Hobart research was the discovery that le-1 dramatically reduces the conversion of one gibberellin, GA20, to another, GA1 (Figure 1; Ingram et al. 1984). As a result, le-1 stems contain much less GA1 than the wild type (Potts et al. 1982; Ross et al. 1992a). Application of GA1, but not GA20, to the le-1 mutant strongly promotes elongation, resulting in plants that resemble the wild type. These results, taken together, indicate that GA1 is the important GA for stem elongation in pea, and that the conversion of GA20 to GA1 (termed 3-oxidation) is a crucial activation step in the GA pathway. This discovery, from the early 1980s, has underpinned all subsequent pea GA research in our laboratory. At about the same time, similar results were obtained and published for maize—another key model species for GA research (Spray et al. 1984).
We then proceeded to characterise the le-1 mutant in more detail and to isolate additional mutants affecting the GA pathway. In so doing, we adapted and developed sophisticated analytical techniques for measuring the minute amounts of GAs present in the plant. It turned out that the le-1 mutation mainly affects stem elongation, and does not reduce—or reduces only slightly—the size of other organs, such as roots, pods or leaves. Is this because GA1 is not important for the growth of these organs or because le-1 does not affect their GA content? Additional mutants helped to answer this question. For example, the lh-2 mutation (Swain and Reid 1992) reduces seed GA content and increases seed abortion (Swain et al. 1993), indicating that GAs are required for normal seed development. Another dwarfing mutation, na (Reid et al. 1983) reduces root GA content, root elongation, and the formation of nitrogen-fixing nodules on the roots (Yaxley et al. 2001; Ferguson et al. 2005), indicating a role for GAs in root growth and nodulation. Both lh-2 and na block GA biosynthesis early in the GA pathway, before GA19 (see Figure 1; Ingram and Reid 1987; Davidson et al. 2003, 2004). The GA content of le-1 roots and seeds was found to be normal, providing an explanation for why there is no phenotypic effect of the le-1 allele on these organs (MacKenzie-Hose et al. 1998; Lester et al. 1999). In pods and leaves, on the other hand, le-1 substantially reduces GA1 levels (Smith et al. 1992; MacKenzie-Hose et al. 1998), but typically without a reduction in size. It appears, therefore, that the level of GA1 might not be the factor limiting pod and leaf growth, or that other factors can compensate for the deficiency of GA1.
One of the most interesting mutants to emerge was sln (Reid et al. 1992). This mutant contains elevated GA1 levels, and its internodes are very long and thin at the seedling stage. We discovered that sln strongly blocks the step, GA20 to GA29 (see Figure 1) in maturing seeds (Ross et al. 1995), resulting in a large accumulation of GA20 by the time the seed is dry and ready to harvest. The accumulated GA20 remains in the seed even when it is stored for months or years, and on germination, moves into the seedling where it is converted to GA1. This GA1 then promotes elongation, resulting in the elongated phenotype. These observations indicate that in young wild-type plants, which are only 30% to 40% the length of the sln mutant, GA1 content limits stem elongation growth. Consistent with this suggestion is the finding that germinating wild-type seedlings contain relatively little GA1 as they emerge from the soil (Ross et al. 1992a).
Molecular Characterization of the Genes
Next, we shifted attention to the molecular characterisation of the genes defined by the mutations. While the 1980s could be termed the "mutant-based" phase of GA research, the 1990s were the "molecular" phase. By the 1990s, it was known that the enzymes catalysing the GA pathway are notoriously difficult to extract and quantify, and so began a trend to bypass the enzymes and to study the genes themselves. It was anticipated that this would answer several important questions, including the molecular nature of mutations such as le-1. Virtually all the genes in the GA pathway have now been isolated and their base sequences published. The interest in characterising these genes was intense. For example, in 1997, we reported the isolation of Mendel′s LE gene (Lester et al. 1997). In the same month of the same year, a similar finding was reported by an independent laboratory (Martin et al. 1997). The genes LE, SLN, LH, NA, and other pea GA genes cloned so far, have turned out to be structural genes encoding enzymes for steps in the GA pathway (Lester et al. 1997, 1999; Davidson et al. 2003, 2004). The LE gene was shown to directly encode the enzyme for converting GA20 to GA1, since this step was efficiently catalysed by the protein produced when LE was expressed in E. coli (Lester et al. 1997). (Since LE encodes a GA 3-oxidase, and the scientific name for pea is Pisum sativum, LE is now also known as "PsGA3ox1.") Determining the sequence of bases in the LE and le-1 alleles showed that the le-1 mutation arose from a G to A substitution at position 685 (Lester et al. 1997; Martin et al. 1997), causing a change from alanine to threonine near the active site of the encoded protein.This change is enough to reduce the conversion of GA20 to GA1 by approximately 95%. Thus, approximately 130 years after Mendel′s paper, the molecular basis of the tall/dwarf difference in his pea plants was finally established (Lester et al. 1997; Martin et al. 1997).
The molecular studies revealed that most GA biosynthesis genes are members of multi-gene families, typically with two to six members. In pea, for example, there are at least two genes that encode "GA 20-oxidase" enzymes (for the step, GA19 to GA20): one expressed in the shoot (Martin et al. 1996), and one in maturing seeds (Lester et al. 1996). The phenomenon of multi-gene families explains why a mutation can affect GA biosynthesis in one organ but not in another. For example, it appears that another member of the 3-oxidase gene family encodes the main enzyme in le-1 roots for converting GA20 to GA1. In contrast, LE is the gene that encodes the predominant 3-oxidase in shoots, and hence, the le-1 mutation strongly affects the shoot phenotype.
Regulation of the GA Pathway
By the late 1990s, we were in possession of the key GA biosynthesis and deactivation genes, as well as the technology (gas chromatography-mass spectrometry) for measuring minute amounts of endogenous GAs. We could then formulate and test hypotheses regarding environmental and internal regulation of the GA pathway, and the interactions between GAs and other hormones. This represented a shift in our research away from characterising new GA mutants, and towards understanding the regulation of GA biosynthesis and deactivation within the wild type. The mutant-based studies had indicated that GA1 regulates growth, but what regulates the level of GA1?
Regulation by Light
The relationship between GAs and the effects of light had been investigated right from the early days of GA research, and in Hobart, we have been studying the problem for at least 20 years. In the past, the long internodes of dark-grown (etiolated) pea plants have often been attributed to a high level of bioactive GA, but when we quantified GAs in continuously dark-grown and light-grown plants, there was no evidence for higher GA1 levels in the former (Weller et al. 1994). However, in the late 1990s there was a new development, when it was reported that in plants that had been grown in the dark and then suddenly transferred to the light, there is a rapid and substantial decrease in the GA1 level (Ait-Ali et al. 1999; Gil and Garcia-Martinez 2000). There is also a substantial decrease in the plants′ elongation rate (O′Neill et al. 2000). It was then shown that after 3–5 days in the light, the GA1 content of the transferred plants increases again—to at least the level found in plants grown continuously in darkness (O′Neill et al. 2000). It appears that, on transfer to light, there is an increase in the rate at which GA1 is converted to GA8 (O′Neill et al. 2000; Reid et al. 2002), and that this is a major reason for the reduction in GA1 level. The drop in GA1 on transfer to light is currently the best example of an environmental effect on GA1-content in pea, and most likely contributes strongly to the accompanying decrease in elongation rate. However, exposure to light also appears to reduce the pea plant′s capacity to respond to GA1, and this is thought to account for the long-term inhibition of stem elongation by light (O′Neill et al. 2000).
In addition to responding to the light regime, the GA pathway is also regulated internally. A well-studied example of internal regulation is "feedback," whereby GA1 and other bioactive GAs regulate steps in their own biosynthesis. Analyses of endogenous GA levels in mutants from several species (Talon et al. 1990a; Hedden and Croker 1992; Ross et al. 1992b; Martin et al. 1996) indicated that the step, GA19 to GA20 (20-oxidation), is down-regulated by active GAs such as GA1. Further evidence was obtained when the genes encoding GA 20-oxidases were cloned: Messenger RNA levels of these genes were shown to be reduced by GA application (Phillips et al. 1995; Martin et al. 1996). Evidence from Arabidopsis thaliana and pea indicated that the 3-oxidation step (for example the conversion of GA20 to GA1) also is down-regulated by active GAs (Talon et al. 1990b; Chiang et al. 1995; Ross et al. 1999). Thus, the capacity of wild-type plants to synthesise GA1 from applied GA20 was found to be less than that of the GA1-deficient mutant na (in which GA biosynthesis is blocked well before GA20). Finally, it was shown that GA deactivation is subject to "feedforward" regulation, whereby expression of GA deactivation genes is up-regulated by bioactive GA (Thomas et al. 1999; Elliott et al. 2001). Thus it appears that, when GA1 levels in the plant are low, GA1 biosynthesis speeds up, while GA1 deactivation slows down, in an attempt to remedy the GA1 deficiency.
Regulation by Auxin
The GA pathway is also regulated by auxin, another key plant growth-promoting hormone. The evidence for this came mainly from experiments with decapitated pea plants—that is, plants from which the "apical bud" had been excised. The apical bud, situated at the top of the main shoot, consists mainly of young, unexpanded leaves. Early in the 1990s, we observed that after decapitation, the remaining stem tissue is essentially incapable of synthesising GA1 from GA20 (Sherriff et al. 1994). Why should removal of the apical bud have this effect? We eventually discovered that applying auxin (in lanolin paste) to the "stump" left by decapitation completely restored the pea stem′s ability to synthesise GA1 (Figure 2; Ross et al. 2000). In contrast, the step, GA20 to GA29, appeared to be enhanced by decapitation and inhibited by auxin (see Figure 1). Cloning of the key GA biosynthesis gene LE and the deactivation gene SLN, enabled us to investigate the molecular basis of these effects. When applied to decapitated plants, auxin up-regulated the expression of LE and down-regulated that of SLN (Ross et al. 2000).
Interestingly, it has been reported also that a different auxin, 4-chloroindole-3-acetic acid, moves from developing pea seeds into the elongating pods where it promotes the step, GA19 to GA20. It appears that 4-chloroindole-3-acetic acid exerts this effect by up-regulating GA 20-oxidase gene expression (van Huizen et al. 1997).
The results from pea shoots (Ross et al. 2000) led us to propose that auxin from the apical bud is necessary for GA1 biosynthesis in stems. It is well known that in many plants, including pea, auxin is transported downwards (basipetally) from the apical bud into, and through, the stem. We have suggested that a major function of this transported auxin is to maintain GA1 levels in the elongating internodes (Ross and O′Neill 2001). When auxin levels are normal in stems, so too is the expression of the LE gene; the GA 3-oxidase enzyme is produced, and GA20 is converted to GA1. This ensures that GA1 can accumulate to the levels normally found in elongating tall pea stems (5 to 20 ng per g), and that growth can proceed in the normal manner. Thus, our model involves a surprisingly simple interaction between the two "classical" plant growth promoters, auxin and GA.
These findings suggest a change in perspective involving auxin action. Given that auxin increases the content of bioactive GA, and that GA is a potent promoter of growth, it seems reasonable to conclude that at least part of the growth response to auxin is mediated by increased GA levels—in other words, that GA is part of the auxin signal-transduction pathway. Evidence for this viewpoint has been obtained by comparing the auxin growth response in excised segments from wild-type and le-1 pea plants. The growth response was strongly reduced in the mutant (Ross et al. 2003), most likely because of its reduced capacity to convert GA20 to GA1, the same step that is strongly up-regulated by auxin.
Potential Interaction with Other Hormones
The brassinosteroids (BRs) are another class of plant growth-promoting hormones, and appropriate levels of bioactive BRs are required for normal stem elongation (Nomura et al. 1997). It has been suggested recently that certain genes involved in auxin signalling are also regulated by BRs (Nemhauser et al. 2004). When it was reported (Bouquin et al. 2001) that BRs can up-regulate the mRNA level (expression) of GA5, a key GA synthesis gene from Arabidopsis that encodes a GA 20-oxidase, GA synthesis genes became candidates for a group of genes that are regulated by both auxin and the BRs. However, in pea, it turned out that LE is not up-regulated by BR; that is, BRs cannot substitute for IAA in regulating the GA pathway (Jager et al. 2005). Consequently, BR-deficient mutants in pea are not deficient in bioactive GAs (Jager et al. 2005).
The confirmation of the BRs as growth-promotor hormones (Li et al. 1996) opened up other discussions about the possibility of effects of auxin, GAs, and BRs on each others′ endogenous levels. However, at this stage, the only interaction with clear physiological significance is the promotion of GA synthesis by auxin. The reverse interaction is much weaker (Ross et al. 2002). Furthermore, it appears that neither the GAs (Jager et al. 2005) nor auxin (Symons and Reid 2004) are required for normal BR synthesis. The effect of BRs on auxin content might be of some importance, because in BR-deficient pea mutants the IAA content of maturing internodes is typically reduced (by two- to threefold), and these mutants do respond to the auxin 2,4-D (MacKay et al. 1994). However, auxin application does not restore a wild-type phenotype to BR mutants, and it appears that the dwarfing effect of BR deficiency is not mediated by auxin deficiency (Jager et al. 2005).
Developmental Regulation: Where Are GAs Synthesised in the Pea Shoot?
The term "hormone" might imply that the compound in question moves from a site of synthesis to a different site, where it acts. In this context, the possible transport of GAs within the shoots of pea and similar species has been the subject of considerable research. The first step was to investigate the site of GA synthesis in the shoot system. One way to tackle this question is to graft together wild-type and GA-deficient shoot material. When young shoots of the extremely GA-deficient mutant na-1 are grafted to mature wild-type stocks, they elongate dramatically and become much more wild type in appearance (Figure 3; Reid et al. 1983). This result indicates that a mobile GA can move into the na-1 shoot from the wild-type tissue, stimulating elongation. In contrast, the elongation of le-1 scions was not promoted by grafting to LE stocks (Reid et al. 1983). Since le-1 is specifically deficient in GA1, the grafting results, taken together, indicate that the mobile GA in grafted na-1 shoots is not GA1 itself, but rather a GA1 precursor, possibly GA20 (Reid et al. 1983; Proebsting et al. 1992). It appears, therefore, that the mature tissue can synthesise GA1 precursors.
|Figure 3 The GA-deficient na-1 mutant elongates dramatically when grafted to a NA stock with mature leaves. The na-1 plant on the left was ungrafted, and remained short. (Click image to enlarge.)|
Further evidence that mature pea tissue synthesises GAs was obtained by showing that this tissue can maintain a constant level of GA19, even though it rapidly metabolises GA19 to GA20 (Ross et al. 2003). The simplest explanation for this observation is that mature tissue continually synthesises GA19. Consistent with that theory is the finding that the GA biosynthesis genes LS, LH, NA, and PsGA20ox1 (encoding GA 20-oxidase) are expressed in mature tissue (Ross et al. 2003; Davidson et al. 2005).
If mature tissue can synthesise GAs, why is the level of GA1 in that part much lower than in the rapidly growing apical region (Smith 1992; Ross et al. 2003)? The answer appears to be that, in mature tissue, GA1 and GA20 are rapidly 2-oxidised to their respective deactivation products, GA8 and GA29 (Ross et al. 2003). In younger tissue, 2-oxidation activity is considerably weaker, and GA1 and GA20 accumulate. Thus, while in pea there is co-localisation of bioactive GA accumulation and rapid elongation, it is probably not correct to say that there is co-localisation of GA biosynthesis and rapid elongation. The mature tissue can synthesise GAs, and, when part of a graft partnership, can export GA1 precursors across the graft union.
This brief overview highlights the value of a multidisciplinary approach to plant hormone biology. Our research has involved techniques from Mendelian genetics, analytical chemistry, biochemistry, molecular biology, and traditional plant physiology. Mutants have been invaluable for studying the phenotypic effects of specific blockages in the GA pathway, and the nature of those blockages was often discovered by rigorous analyses of endogenous GA levels. Modern molecular techniques have become indispensable for delving into environmental and endogenous regulatory mechanisms. Nevertheless, the questions answered by modern techniques have often originated in the traditional plant physiology of decades ago, and the recent progress would not have been possible without the groundbreaking work that originally established the GA pathway (e.g. Sponsel and MacMillan 1977).
In conclusion, the GAs are essential for normal growth and development in pea, and the GA pathway is tightly regulated by a number of factors. Each step is typically controlled by a multi-gene family, although not all members of that family are expressed in the same tissue. Bioactive GAs down-regulate their own biosynthesis and up-regulate their deactivation, and auxin is required for normal GA biosynthesis in stems. The nature of the light regime also exerts dramatic effects on the pathway, and on stem elongation.
I would like to thank Andre Phillips and Jennifer Smith for preparing the figures, and Damian O′Neill and Jim Reid for their comments on the manuscript.
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