T H E

Euphytica 25 (1976) 167-174

G E N E T I C S OF N A K E D OATS (AVENA NUDA L.)

G. J E N K I N S and P. R. H A N S O N

Plant Breeding Institute, Trumpington, Cambridge, England

Received 17 June 1975

INDEX WORDS

Arena nuda, oats, naked grain, multiflorous spikelets, genetics.

SUMMARY

The inheritance of the character complex of naked grain and multiflorous spikelets was studied in a diallel set of crosses comprising five varieties of naked oats (Avena nuda) As 78, Manu, Caesar, Nuprime and AJ86/2/1 - and one variety of husked oats (A. sativa), Marls Oberon. In the F1 generation the distribution of multiflorous spikelets was in all cases similar to that of the mid-parent. Crosses between the varieties of A. nuda produced only naked grain on plants in the Fa and F2 generations, indicating that 'nakedness' in the varieties studied was determined by the same loci.

The three-gene model proposed by MOULE (1972) for the determination of A. nuda characters was inadequate to account for the observed F2 segregation in naked × husked crosses. An extension of this model is proposed to include a third modifying gene, N3, which in the homozygous dominant condition Produces the husked phenotype when the principal gene, N, is heterozygous. The model assumes complex epistatic relationships between the three modifying genes NI, N2 and N3. Published information and further experimental data suggest that the genotype NN -- N3N3 is uncommon. The expression of the genes determining nakedness was greatly influenced by the environment.

INTRODUCTION

The potential agricultural value of naked oats (Arena nuda L.) has been discussed elsewhere (JENKINS, 1968). Although these are fully interfertile with the more ex- ensively cultivated husked oats (A. sativa L.) they differ in the morphology of the inflorescence. In naked oats the spikelets are typically multiflorous with elongated rachilla segments, in contrast to the compact spikelets of husked oats which normally contain only two or three functional florets. The caryopsis in naked oats is free thresh- ing and separates easily from the thin membranous lemma and palea which, in husked oats, become thick and lignified and tightly enclose the grain at maturity. Naked grains, elongated rachillae and multiflorous spikelets comprise a character complex which appears to be pleiotropically inherited. In early panicle ontogeny, however, the spikelets of both naked and husked oats are multiflorous (BONNCT, 1966), SO it appears that, in the latter form, a switch gene operates to inhibit the further develop- ment of the upper florets initiated in the spikelets. The panicles of F 1 plants of naked x husked varieties are structural mosaics in which the earlier formed spikelets at the top of the panicle are multiflorous, with a preponderance of sativa-type florets at the base. Nakedness is therefore incompletely dominant and the F 2 generation is composed of some fully husked and some fully naked plants with a wide intermediate category of mosaic phenotypes differing greatly in the proportion of nuda-type spikelets and naked grains.

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The earlier literature on the genetic control of nakedness has been reviewed by JENSEN (1961) and MOULE (1972). Early hypotheses of control by a single incomple- tely dominant gene proved inadequate to account for later results and varying num- bers of modifying genes have subsequently been proposed. The most recent com- prehensive analysis is that of MOULE, who proposed an incompletely dominant prin- cipal gene, Nn, which 'tends to initiate' the naked phenotype. It was further proposed that the expression of this gene, when homozygous dominant or heterozygous, is modified by the action of two secondary genes, Nln I and NEn2, also incompletely dominant in their effect. In all cases, the principal gene, nn, when homozygous re- cessive, produces the husked phenotype. MOULE defined three phenotypic classes: naked ('nu'); semi-naked or mosaic ('mi-nu') and husked ('v6tu'). The possible genetic situations arising in homozygous lines are:

NN N1N1N2N 2 and NN N1NanEn 2 ~ naked NN nlnjN2N2 and NN nlnln2n2 --~ mosaic n n - - - ~ husked.

Some difficulty was encountered by MOULE in applying this model to certain sit- uations and the possibilities of multiple allelism, epistatic effects and variation due to the genetic background, were suggested. The work described here was initiated be- fore the publication of MOULE'S paper and the results obtained have necessitated a reconsideration of his proposed 3-gene model.

M E T H O D S A N D M A T E R I A L S

A full diallel set of crosses was produced by hand-pollination in the glasshouse of the following six varieties, of which the first five are classified as A. nuda."

Variety As 78 Manu Caesar Nuprime AJ 86/2/1

Maris Oberon

Pedigree unknown Swedish black oat x Chinese naked USA naked x Breustedt's Harley Laurel x Ariane (Avon x James) x Astor

Manod x (Astor x AB203/187)

Source Leningrad, USSR Germany Germany France Plant Breeding Institute, Cambridge Plant Breeding Institute, Cambridge

The parental line AB203/187 itself has the pedigree F 4 (Stormont Iris × Blenda) x (Cc4146/4 x Condor); Cc4146/4 is an accession of the Welsh Plant Breeding Station, Aberystwyth and is a presumed natural hybrid of A. sterilis x A. sativa.

The F1 and F z generations were grown together in a large, naturally lit glasshouse during the summer of 1972. The F1 diallel set with its parents was grown in a ran- domized block trial with ten replications, each plot consisting of a single plant in a 12.5-cm diameter pot. The Fz generation was planted by crosses in blocks of similar pots, also containing one plant each, with the parents interspersed as controls. At maturity the Fj plants and parents were harvested on roots while from each F2 plant

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G E N E T I C S OF NAKED OATS

the main panicle was harvested for further inspection. The panicle structure of the F 1 plants and parents was analysed in detail by recording, at each whorl on the main panicle, the total number of spikelets and the number which were multiflorous. In addition, the total number of grains and the proportion of naked grains were recorded. For the F2 panicles, counts were made of total spikelet number, total grain number and the number of naked grains.

Progenies of F2 plants of the A. nuda x A. sativa crosses but not of the A. nuda × A. nuda crosses were sown in the field in March 1973. Each progeny was represented by a row of 20 plants spaced 5 cm apart with 15 cm between adjacent rows. At harvest, the main panicle was taken from each plant and subsequently threshed gently by hand. The plants were roughly classified as having 100, 75, 50, 25 or 0% naked grain.

For reasons discussed below, a random sample of F 3 lines, representing the plants classified as husked in the F2 population of the cross. As 78 × Marls Oberon was grown in the glasshouse in 1973. These F 3 plants were intercrossed at random by normal hand pollination. In this way 56 F 3 plants representing 32 F2 plant progenies were intercrossed and the resulting F1 seeds were planted out in the glasshouse for observation in 1974.

Five other husked varieties from which additional crosses to the naked variety As 78 were made comprised:

Variety Pedigree Maris Tabard Cc4146/4 x Condor 2

Source Plant Breeding Institute, Cambridge

Avon (Mulga x Burt's Early) x (Mulga x Luggan) W. Australia

Sierra Nullisomic line x A.fatua California, USA Blenda Star x Eagle Sweden Black Tartarian unknown obscure

The F 2 populations of the As 78 crosses listed above were also sown in the field as single plants placed 5 x 15 cm apart in March 1973. At harvest the main panicle from each plant was removed for analysis as described above.

R E S U L T S A N D D I S C U S S I O N

F 1 generation. All crosses between A. nuda varieties produced typical naked-grained F 1 plants. The F1 plants of crosses between the A. sativa variety (Maris Oberon) and the five A. nuda varieties had typical mosaic panicles with multiflorous, naked-grained spikelets in the upper whorls and varying proportions of 2-3 floret spikelets, bearing husked grain, mostly concentrated in the basal whorls. The distribution of spikelet types within the panicles of F1 plants of these A. nuda × A. sativa crosses was gen- erally intermediate between those of the respective parents.

F2 generation. No fully husked phenotypes were observed in any of the crosses between A. nuda varieties in F z populations numbering several hundred plants in each case. It appeared therefore that the same genes determined nakedness in the five varieties chosen for study.

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G. J E N K I N S AND P. R. H A N S O N

Nurc,ber of plants in each class

180

'°t ,oo 140

130]

';]

60

1

0 0:1- 11- 21- 31- 41- 51- 61- 71- 81- 91- 10 20 30 40 50 60 70 80 90 100

Naked grains (%)

Fig . 1. Frequency distributions of Fz phenotypic classes for five A. sativa x A. nuda crosses. x Marls Oberon x AS 78; A Maris Oberon x Manu; © Marls Oberon x Caesar; • Marls Oberon × Nuprlme;e Marls Oberon x AJ 86/2/1.

Examination of the F 2 populations of the A. nuda × A. sativa crosses showed first, that the proportion of fully husked phenotypes was much higher than in most pre- viously reported studies and secondly, that the phenotypes not classified as fully husked, varied widely in the proportion of A. nuda type spikelets borne. There was no evidence of reciprocal differences and the reciprocal cross data were therefore pooled for subsequent analysis. The frequency distribution of plants with different proportions of naked grains showed effectively continuous variation with little sug- gestion of the bimodality reported by CLAMOT (1969) (Fig. 1). In subsequent analyses it was therefore decided to define only two phenotypes: 'husked' in which the spikelet type was entirely like that of A. sativa, with all grains husked, and 'naked' which included plants with widely varying proportions of multiflorous spikelets and naked grains.

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GENETICS OF NAKED OATS

Table 1. Segregation of F2 populations ofA. sativa (Marls Oberon) × A. n u ~ crosses.

A. nuda parent Observed segregation Proposed ratio

naked husked 9:7 35:29

Z z p Z z p

AS 78 179 144 0.09 0.8-0.7 0.07 0.8-0.7 Manu 194 166 0.82 0.5 -0.3 0.09 0.8 0.7 Caesar 123 111 1.28 0.3 ~0.2 0.43 0.7-0.5 Nuprime 195 181 2.94 0.10-0.05 1.21 0.3 0.2 AJ 86/2/1 161 147 1 . 9 8 0.20~0.10 1.73 0.5-0.3

The F2 segregations in these categories for all five crosses (Table 1) do not remotely fit a ratio of 3 naked: 1 husked, implying, therefore, segregation at more than one locus. The simplest model which fitted the data was that of two complementary dominant genes. Superficially, this could be reconciled with earlier hypotheses of the segregation of a single incompletely dominant gene by assuming that the A. sativa variety, Maris Oberon, is recessive for a second gene which must have been dominant in other A. sativa varieties used by previous workers.

However this simple 2-gene model is not tenable on several counts. First, the random intercrossing of fully husked F 3 plants would be expected to produce F a plants with mosaic panicles in the proportion 8 : 49, i.e. approximately 1 : 6. Inter- crossing 56 such F 3 plants from the cross As 78 x Maris Oberon produced 178 plants none of which had any nuda characteristics, whereas the population size required for a 99~o probability of obtaining at least one plant with the proposed characters is 25 (MATHER, 1938). Secondly, it is essential to the hypothesis of two complementary genes that the husked F 2 plants would breed true. However, it was subsequently noted that a proportion of the husked F 2 progenies segregated naked plants. Thirdly, any genetic model proposed must also take into consideration the total evidence available but a hypothesis of two complementary genes is not com- patible with the results of the recent detailed study by MOULE (1972). To compare our results with those of MOULE it is necessary to merge his naked and intermediate classes ( 'nu' and 'mi-nu'). On this basis, a ratio of 3 (naked + mosaic): 1 husked would be obtained if only the principal gene, Nn, were segregating. MouLE's inter- pretation of situations in which either or both of the modifiers, N ln I and N 2 n 2 ,

are segregating is complicated but would result in ratios of 5 : 3 or 23 : 9 depending on whether the F 2 genotypes Nn n l n l N 2 N 2 and Nn n ln lN2n 2 give husked or naked phenotypes. To accommodate both possibilities, MOULE postulated the existence of alleles in different husked parents which could modify the F2 segregation ratios ob- tained. None of o u r F 2 data fit these ratios and in accepting the basic validity of MOULE'S model we have found it necessary to postulate a third modifying gene. This gene, denoted as N 3, would operate in the reverse direction to MOULE'S modifiers N 1 and N 2 so that when homozygous and dominant it determined the production of fully husked grain, when the principal gene N is heterozygous. In the homozygous

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G. JENKINS AND P. R. HANSON

recessive condition n3n3, the gene would be hypostatic to a dominant allele at any of the other loci. The model requires rather complex assumptions of epistasis when the principal gene (Nn) and the third modifier (N3n3) are heterozygous. These are best summarized as follows:

Nn Nln I nzn 2 N3n 3 or Nn nln I N z n 2 N3n 3 --~ husked but Nn Nln I N 2 n 2 N 3 n 3 o r Nn N1N 1 n2n 2 N 3 n 3 or Nn nln I N 2 N 2 N 3 n 3 --* naked

It is fundamental to the model that NN . . . . is always naked and nn . . . . is always husked, regardless of the alleles present at the other loci.

This genetic model would result in an F 2 segregation of naked to husked in the ratio 35 : 29. The F2 segregations of the five observed crosses of naked oats with Maris Oberon gave reasonable fits to this expectation (Table 1).

F3 generation. A random sample of F 2 plant progenies would be expected to segregate on the basis of our four-gene model in the proportions indicated in Table 2. It is im- mediately apparent that the field sowing of F 3 lines, necessitated by the large volume of material involved, exerted a profound effect on the expression of the nuda charac- ters, resulting in a major shift to the husked phenotype. A small proportion of progeny derived from naked F2 plants produced only husked phenotypes which, on theoretical grounds, could not be expected. It is well established that the environment modifies the expression of the nuda characters (MARTZENITZYNA, 1950; JENKINS, 1973). More especially, BOLAND & LAWES (1973) have recently demonstrated that glasshouse con- ditions enhance the expression of nakedness compared with field sowing. The small proportion of completely husked progenies of naked F 2 plants might therefore be attributed to the effect of the environment together with some sampling error and, possibly, misclassification. The F3 generation results obtained neither confirm nor disprove the proposed four-gene model but they emphasise the need to conduct prog- eny tests in the same environment as that used to test the F2 generation wherever possible.

Additional crosses. The need to postulate a third modifying gene arose from the F 2 segregation resulting when Maris Oberon was used as the husked tester variety. It

Tabel 2. Segregation ofF2 progenies from A. sativa (Maris Oberon) × A. nuda crosses.

F 2 c l a s s F2 progeny class Expected proportion

Observed proportion in progeny class (number of plants) in A. nuda parent

As 78 Manu Caesar Nuprime

Husked all husked 0.25 0.45 (146) 0.47 (166) 0.47 (71) 0.51 (87) segregating naked-husked 0.20 0.05 (15) 0.03 (10) 0.01 (2) 0.08 (14)

Naked all naked 0.25 0.01 (2) 0.03 (9) 0.03 (5) 0.03 (5) segregating naked-husked 0.30 0.40 (131) 0.32 (113) 0.42 (63) 0.38 (66) all husked 0.00 0.09 (29) 0.16 (58) 0.06 (10) 0.05 (9)

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GENETICS OF NAKED OATS

Table 3. Segregation of F 2 populations of A. nuda ( AS 78 ) × A. sativa crosses.

A. sativa parent Observed segregation Best fitt Z 2 p naked husked

Maris Tabard 273 190 5 : 3 2.47 0.24). 1 Avon 400 159 23 : 9 0.03 0.94).8 Sierra 112 55 5 : 3 1.48 0.34).2 Blenda 543 246 23 : 9 3.64 0.14).05 Black Tartarian 138 58 23:9 0.21 0.74).5

seems possible, therefore, that the presence of the gene NaN a as the dominant allele in A. sativa varieties is uncommon. Further crosses of the primitive A. nuda genotype, As 78, were made to husked varieties of widely diverse origin to explore this sup- position. The derived F 2 populations were sown in the field in the same season as the F a material discussed above and the observed segregations are given in Table 3. It may be seen that segregation in the five crosses was compatible with Moule's 3-gene model, although the fit for the Blenda cross was poor.

No supporting evidence for the postulated third modifier was therefore provided by this limited set of crosses. It is of interest, however, that the cross with Maris Tabard produced a higher proport ion of husked to naked F 2 plants than any of the others, because this variety shares with Maris Oberon a common parent of obscure origin. The fit for the 4-gene model for the Maris Tabard cross was less good ( Z 2 =

3.42, p ---- 0.1 - 0.05) than that for the 3-gene model (Table 3) but would not exclude a segregation ratio of 35 : 29 as required.

CONCLUSIONS

Hexaploid naked oats have apparently been derived from a narrow genetic base (JENKINS, 1968). In view of this it is not surprising that the same loci were found to determine nakedness in the varieties studied.

The situation of a major 'switch' gene, N, which is modified in its expression by three other loci, provides an interesting parallel with the vulgare factor Q for basal floret fertility in Triticum which is reinforced by a factor, Bs, located on a homeolo- gous chromosome and which, in turn, interacts with a polygenic system P (FRANKEL, 1975; FRANKEL 8~ ROSKAMS, 1975). However, diploid forms of naked oats are known and the complex operation of three factors has been propounded at that level so that it is unnecessary to invoke a homeologous series (EMME 8Z MORDVINKINA, 1939). No naked oats have been reported at the tetraploid level.

The existence of a third modifying gene in hexaploid naked oats has occasionally been suggested previously (LEBEDEV, 1930; CLAMOT, 1969) but we believe this to be the first definite proposal of its mode of action. The proposal is also compatible with the basic model proposed by MOULE. It would seem that the frequency of the pro- posed allele N 3 is lOW and further test crosses of naked oats with a range of husked forms need to be made.

Moule suggested the possibilities of multiple allelism at some of the modifier loci

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G. JENKINS AND P. R. HANSON

and of some interaction with the genetic background. Taking into consideration also the known influence of the environment on the expression of the nuda characters and the epistasis involved in our four-gene model it is apparent that very complex situations can result. In breeding terms, MOULE'S suggestion that the best method for genetic improvement of naked oats is by simple hybridisation, followed by selec- tion for the maximum expression of nakedness, is reinforced by our observations.

REFERENCES

BOLAND, P. & D. A. LAWES, 1973. The inheritance of the naked grain character in oats studied in a cross between the naked variety Caesar and the husked variety BO 1/11. Euphytica 22: 582 591.

BONNETT, O. T., 1966. Inflorescences of maize, wheat, rye and oats: their initiation and development. Bull. Ill. agric. Exp. Stn 721 : 92-105.

CLAMOT, G. 1969. Etude de l'h6r6dit6 du caract6re 'Grain nu ' chez l 'avoine. Bull. Rech. agron. Gembloux IV: 323-338.

EMME, E. K. & A. I. MORDVINKINA, 1939. Hybrids of the 14-chromosome naked oats. Bull. Acad. Sci. URSS S6r. Biol. 530-540.

FRANKEL, O., 1975. Base-sterile speltoids: the location of the Bs gene of Trtiticum aestivum. Proc. R. Soc. London, B 188, 163-166.

FRANKEL, O. ~,~ M. ROSKAM, 1975. Stability of floral differentiation in Triticum. Proc. R. Soc., Lond. B 188: 139-162.

JENKINS, G., 1968. Naked oats. N.A.A.S .q . Rev. 79: 120-126. JENKINS, G., 1973. The effect of sowing data and photoperiod on panicle morphology in naked oats.

Ann. appl. Biol. 73: 85-94. JENSEN, N. F., 1961. F. A. Coffman (Ed.), Oats and oat improvement. Agronomy 8: 188. American

Society for Agronomy, Madison, Wisc. LEBEDEV, V. N., 1930. Factorial analysis of characters distinguishing Avena nuda L. from A. Sativa L.

I. Coarseness of the outer floret paleae. (Russian.) TrudS, Belotserk. Selek. STantsii 5: 3 23. MARTZENITZYNA, K. K., 1950. On hybrids of naked and common oats. (Russian.) Agrobiologiya: 43-59. MATHER, K., 1938. The measurement of linkage in heredity. Methuen, London, pp. 132. MOULE, C., 1972. Contribution a l '6tude de l'h6r6dit6 du caract6re 'grain nu ' chez l 'avoine cultiv6e. Annls

Am61. Pl. 22 : 335-361.

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