Complementation in Tryptophan Biosynthetic Pathway

Tryptophan biosynthesis: The material that follows is not included in the main part of chapter 6. However, much of the pathway that is involved is illustrated in figure 6.15, which goes with problem 13. The tables that follow were employed by Susan Dutcher in the version of MCDB 2150 that she taught at the time I first began teaching this course. Auxotrophic mutations that require tryptophan for growth were tested for their ability to grow on a series of known precursors for the biosynthesis of tryptophan. Mutants were found that were blocked at five different steps leading from chorismate (the first precursor in the series) to tryptophan. The patterns of which intermediates would or would not support growth of each mutant strain agreed exactly with the known pathway for biosynthesis of tryptophan. The overall pathway of tryptophan biosynthesis in Neurospora is chorismate --> anthranilate --> phosphoribosyl anthranilate --> 1-(o-carboxyphenylamino)-1-deoxyribulose-5-phosphate --> indoleglycerol phosphate --> tryptophan. The enzymes involved in each step are shown below in italics. A crudely simulated arrow head (\:/) has been used to depict the reaction arrow for each catalytic step because of lack of an appropriate vertical arrow symbol in html.

Growth characteristics of mutants: The table that follows shows the growth of seven mutant strains (M1 - M7) of Neurospora on TRP and the its biosynthetic intermediates.

Substrate
M1
M2
M3
M4
M5
M6
M7
CHOR
-
-
-
-
-
-
-
ANTH
-
+
-
-
-
-
-
P-ANTH
-
+
+
-
+
-
-
CPADP
+
+
+
-
+
_
_
IGP
+
+
+
-
+
+
-
TRP
+
+
+
+
+
+
+

Complementation analysis was done by fusing hyphae such that the cultures contained nuclei with two different types of mutations. In cases where each nucleus was able to code for the enzyme whose gene was mutated in the other nucleus, phenotypically wild type growth was obtained. Analysis of the seven mutant strains yielded the results shown in the table below (mut = mutant phenotype, requiring tryptophan for growth; wt = wild-type phenotype, capable of growing without added tryptophan or any of its biosynthetic intermediates):

M1
M2
M3
M4
M5
M6
M7
M1 +
mut
wt
wt
wt
wt
wt
wt
M2 +
mut
wt
wt
wt
wt
wt
M3 +
mut
wt
mut
wt
wt
M4 +
mut
wt
wt
wt
M5 +
mut
wt
wt
M6 +
mut
wt
M7 +
mut

Conclusions: All seven mutations fail to complement themselves, as expected. Mutations 3 and 5 fail to complement each other, indicating that both affect the same peptide chain in the enzyme, anthranilate phosphoribosyl transferase, which is needed for synthesis of P-ANTH. Mutations 4 and 7 do complement each other, despite the fact that both cause loss of tryptophan synthase activity. This is consistent with the fact that tryptophan synthase is known to be composed of two subunits designated alpha and beta. Thus, complementation analysis precisely verifies the biosynthetic pathway and allows identification of mutations that affect the same step as well as identification of enzymes that appear to be composed of two or more subunits.

Suicide substrates: Genetic studies on tryptophan biosynthetic pathways have also been done in Arabadopsis, a small flowering plant. In this case, a suicide substrate was used to select for mutant strains. The enzymes that convert anthranilate to tryptophan can also convert 5-methylanthranilate to 5-methyltryptophan, which is incoprorated into proteins like tryptophan, but results in non-functional proteins, such that the plant does not survive. 5-methyltryptophan also blocks de novo synthesis of tryptophan by feedback inhibition of anthranilate synthase, thus preventing biosynthetic tryptophan from competing with the 5-methyltryptophan. Plants with mutations blocking any steps in the pathway between anthranilate and tryptophan can thus grow in the presence of 5-methylanthranilate when also supplied with small amounts of tryptophan, whereas those that are not blocked will make enough 5-methyltryptophan to inhibit growth even in the presence of the small amount of added tryptophan. This provides a powerful way to select for tryptophan auxotrophs in Arabadopsis.

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