Peas (Pisum sativum L.)

ELSEVIER

Field Crops Research 53 (1997) 111-130

Field Crops _ Research

Peas ( Pisum sativum L.) R. Cousin

*

INRA, Station de Gdn~tique et d'Am~lioration des Plantes, Versailles, France

1. Introduction Peas have been grown as an important source of animal feed and human food for many centuries. Over this time, pea has been selected for these uses. Several thousand varieties exist throughout the world. They can be classified into the following categories: • field peas, providing forage for animal feed; • market peas, from which pods are harvested for human consumption as a fresh vegetable; • vining peas, for canning or freezing; • dried peas, partly for human consumption but mostly for animal feed. Considerable developments have been made with dried peas over the last decade in order to further satisfy the needs concerning animal feed. World production of dried peas is currently estimated to be 16 million tons. The primary areas of production are the former USSR (7.3 MT), Europe (4.8 MT; of which France produces 3.2 MT) and China (1.6 MT). The world average yield per hectare was 1.82 tons and was greatest in France (4.95 tons ha -1) and least in India (0.92 tons ha -1) (FAO, 1991). However, the yield within different countries was unstable. Consequently, many characters have to be improved in order to satisfy the developing needs of growers, processors and feed manufacturers.

* Corresponding author.

2. Origin and general botany The pea has been known since antiquity. Theophrastus (1961), in his book Enquiry into plants translated in English by Arthur Hort, mentions traces of pea much earlier than 300 years B.C. He describes several species of legumes and especially the 'Pea' and reveals that peas were used for fodder and human food. The pea crop was known in the prehistoric age in Europe. Peas dating from the Stone Age have been discovered in the excavations at Aggetelek in Hungary and in lake-dwellings in Switzerland (Fourmont, 1956). In France, peas exhumed from dwellings in the Bourget lake belong to the Bronze Age, (1000-2000 B.C.) and are assumed to have been grown by Aryan people (Gibault, 1912). Recently, Smartt (1990) in his book Grain Legumes: Evolution and Genetic Resources, indicates that peas date back to 7000-6000 B.C. Erskine et al. (1994) mentions that peas were rare at Jarmo, Iraq (6750 B.C.), while they constitute the prevalent pulse at a Neolithic site at Erbaba in Turkey (5800-5400 B.C.). Peas probably originated in Abyssinia and Afghanistan, with areas in the Mediterranean area colonized later. From these areas the pea spread to other parts of Europe and Asia. Botanists have described wild species which differ from cultivated peas only by morphological characters. Sometimes these types have constituted different species original area: P. formosum, P. transcaucasicum, P. abyssinicum, P. aethiopicum, P. arvense; but, most

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112

R. Cousin/Field Crops Research 53 (1997) 111-130

frequently, they are considered as belonging to the Pisum sativum species (Fourmont, 1956). These wild species often have tall, (more than 2 meters), slender and branched stems, purple or pink flowers and small pods producing a small quantity of seeds with colored coat. P. elatius and P. abyssinicum have distinct toothed leaflets and stipules. P. elatius has colored flowers, lilac-blue standards, dark purple wings and maroon veiny brown seeds. P. abyssinicum has pink flowers and dark purple seeds. P. fulvum may have two fructification types, a normal one located in the upper part of the plant, the other very peculiar with very short basal branches which push the pods slightly into the ground. P. humile is characterized as a medium sized climbing species with dentate leaf margins and light blue flowers. The two forms of cultivated pea, the field pea (P. arvense L.) and the garden pea (P. sativum L.) are sometimes regarded as separate species. There is very little justification for this since they can be crossed readily and are quite inter-fertile. It seems probable that the garden pea was derived by selection from the field pea (Smartt, 1976). Based on analyses of morphology, cytogenetics and hybrid performance, Ben-Ze'ev and Zohary (1973) concluded that P. fulvum is a fully divergent species, whereas P. humile, P. elatius and P. sativum form a single species complex. Other researchers show that Pisum is monospecific, suggesting that the differences observed for P. fulvum relative to the other pea taxa are more a matter of degree than the basis for a distinct species (Wellensiek, 1925; Hedrick, 1928; Lamprecht, 1966; Blixt, 1974). Davies (1974), Marx (1977) and Palmer et al. (1985) agree with the conclusion that P. humile is the wild progenitor of the cultivated pea. Recently, Hoey et al. (1996) have confirmed this origin through a phylogenetic analysis based on certain morphological characters and RAPD markers. In the same way Samec and Nasinec (1996), using also RAPD Technique and dendrogram representation, analyze relationships among lines of P. sativum ssp. elatius, P.s. ssp. aruense, P.s. ssp. humile and P.s. ssp. sativum. 2.1. Plant biology and controlled pollination

The pea flower is typical of the Papilionaceae family. The corolla contains five petals: the standard,

two wings and a keel formed as the result of fusion of two petals surrounding ten stamens and one style. The pea is cleistogamous and must be considered as a strictly self-fertilizing species, though Xylocopa and Megachile do visit pea flowers and can be responsible for natural hybridizations. Thus, some genetic mixing can take place without the intervention of pea breeders. Natural populations and varieties consist of genetically stable plants. All cultivated pea varieties are pure lines. In order to obtain hybrid varieties, it would be necessary to find mutants with open flowers, a male sterile source and an efficient pollen carrier. Artificial seed production might also be considered after micropropagation of hybrid seeds. But, due to the complexity of these techniques and the profitability which is yet to be proven, it seems probable that pure line varieties will continue to be used. 2.2. Yield and plant characteristics

Pea plants exhibit an indeterminate growth habit. The first nodes, some of which give rise to branches, are vegetative, while subsequent nodes are reproductive. Generally two flowers, from which the pods develop, are present at each reproductive node. The number of seeds per pod depends on the variety and on the environmental conditions. There is a large genetic variability for number of branches, pods, seeds per pod, thousand-seed weight, leaf area, height of the plant. However, when crosses are made which attempt to improve on, and combine these traits, yields are often reduced. In order to better define the characters limiting yield, yield variations have been studied for a range of varieties in a progressive multiple regression analysis involving variations in a range traits. In this analysis only thousand seed weight, seedling vigor and harvest index were positively correlated with yield, though correlation coefficients were low, while a number of the traits studied were negatively correlated with yield (Table 1) (Cousin et al., 1985). From this data it appears that when vegetative growth is vigorous, there is increased interplant competition and yield suffers. Reduction in leaf area and plant height to produce smaller, more highly branched plants and increasing of the thousand seed weight favors yield. A similar analysis undertaken on winter

R. Cousin/Field Crops Research 53 (1997) 111-130

113

Table 1 C o r r e l a t i o n c o e f f i c i e n t s b e t w e e n s e e d y i e l d a n d d i f f e r e n t p l a n t c h a r a c t e r s , 1977, 1978, 1980, 1981 a n d 1 9 8 2 at V e r s a i l l e s . ( C o u s i n et al., 1985) Character

Year 1977

1978

1980

1981

1982

- 0.39 b

-- 0 . 6 6 b

-- 0 . 7 0 b

-- 0.35 b

-- 0 . 2 4

0.23 0.24

- 0.28 0.49 b

- 0.19 0.41 b

- 0.33 b 0.42 b

- 0.01 -0.18

- 0.04 -0.41 b

- 0.02 --0.41 b

0.16 0.15

--0.10

0.35 b

Plant Height (Sum heat unit) 2 Thousand-seed weight Number of seeds per pod Leaf area Seedling vigour (dry matter)

0.27 b

0.44 b

N u m b e r o f fertile b r a n c h e s at the top

0.19

0.31

0.09 0.33 b - 0.08 --0.11 0.34 b

0.18 -0.18

at t h e b o t t o m Harvest index

0.36 b

0.05 0.37 b

-0.34

b

0.29

Main stem Number of pods

- 0.24

- 0.60 b

-- 0.28 a

-- 0 . 0 7

-- 0 . 4 0 b

Number of seeds

-0.16

-0.57

--0.27 "

0.01

--0.38 b

b

S i g n i f i c a n t at 5 % . b S i g n i f i c a n t at 1%. a

peas also revealed the necessity of reducing the leaf area. But winter peas may be taller, and seed size seems to be less important. Seeds may be smaller and more numerous. Decrease of leaf area is undoubtedly the genetic improvement which will most improve productivity and stand. Several genes are available that reduce leaf area (Fig. 1): 'af' gene converts leaflets to tendrils and gives 'semi-leafless peas'; 'st' gene gives reduced stipules, and combined with the 'af' gene results in leafless peas; 'Rogue' gene reduces the leaflet and stipule size, and makes them erect like hare's-ears. Of these the 'semi-leafless' type appears to be the most promising. The 'af' gene induces a 40% decrease in leaf area, with the leaf area better distributed along the stem, chiefly at the level of the fertile nodes. This contributes to better light penetration through the canopy. Isogenic lines yield 0 to 20% more than normal foliage lines. These lines also show better standing ability which facilitates mechanical harvesting. These analyses reveal that it is necessary to reduce most of the yield factors excepted thousand

seed weight. This leads to the concept of reducing the biomass in order to increase seed yield. 2.3. Biomass and seed production In order to study the relationships between biomass production and seed yield, the dry matter has been measured in different organs of the plant during plant development. This study, carried out on several varieties, reveals that the genetic variability exists for biomass production and translocation capacity. For instance, results obtained with eM, Frisson, Finale and 776 show this variability (Fig. 2): • eM, very early line, has low biomass, good translocation and medium yield; • Frisson and Finale, intermediate flowering cultivars, have medium biomass production, better translocation capacity and higher seed yield; • 776, late line, has the highest biomass production and the lowest translocation capacity. The seed yields becomes very low. When biomass production becomes too high, interplant competition reaches a high level and the seed yield decreases. Thus the translocation capacity

R. Cousin~Field Crops Research 53 (1997) 111-130

114

IBB Seeds I--1 Pods m= Stems and leaves

a

d

409

508

564

658

763

899

1001

1169

409

508

564

858

763

829

1001

1169

1255

t370

1485

409

508

564

558

763

899

1001

1189

1255

1370

1485

4O9

508

564

658

763

899

1001

1166

1255

1370

1485

b

•

f

Fig. 1. Different morphological types of pea leaves. (a) Normal leaf. (b) Semi-leafless or 'afila', 'af' gene transforms the leaflets into tendrils. (c) Leafless, combination of 'af' and 'st' genes. The 'st' gene causes reduced stipules. (d) Acacia-type, the 'tl' gene transforms the tendrils into leaflets. (e) Combination of 'af' and 'tl' genes. (f) Hate's ear, the 'rogue' gene reduces the width of the leaflets and stipules and makes them erect.

may be a determinant factor for yield. Utilization of 15N reveals that the decrease in dry matter of the vegetative organs results essentially from the remobilization of nitrogenous substances. The utilization of 15N applied at different stages of plant growth, has shown that nitrogen is stored in temporary organs, then transferred to young structures of the plant and finally remobilized towards the seeds. Genetic variability exists for the translocation capacity. The study of two genotypes indicated that the remobilization began early and was greater for 'Frisson' than to line 833 (Fig. 3) (Atta, 1995). Differences in remobilization from different nodes can explain the differences in seed yield between 776 and 'Finale'. For the high yielding 'Finale', the dry matter was remobilized from all nodes of the

Cumulativedegreedaysfromsowing Fig. 2. Dry matter accumulation in different organs during plant development. (Atta, 1995).

plant once growth bad ceased. In contrast, for the late line 776, remobilization was great only from nodes located around the first fertile node, when

Line

~

833

Frlsson

,o 2 VS

FIo.

i

Filfing Maturity

1111 I

I

VS

I

FIo,

I

I

Filing Matudty

• Seeds

[ ] Lowerleaves

[ ] Stems

[] Pods

[] Upperleaves

[ ] Roots

Fig. 3. Distribution of 15N in different organs during plant development following labeling at the vegetative stage. (Atta, 1995).

115

R. Cousin/ FieM Crops Research 53 (1997) 111-130

vegetative growth was not completely over (Fig. 4) (Atta, 1995). Biomass production and remobilization are linked to nitrogen fixation. Thus, it is necessary to know the genetic variability for nitrogen (N 2) fixation.

reduction activity (ARA) method (Balandreau and Dommergues, 1973). The duration of the fixation period was the same for all varieties, irrespective of flowering date. It began one month after sowing and lasted up to two months. Consequently, for an early variety, N 2 fixation continued during seed development while, for a late variety, it stopped after flowering. Moreover, if sowing was delayed, fixation activity increased more rapidly while the duration decreased. In 1991, a one month delay in the sowing

2.4. Nitrogen fixation

Varietal differences in nitrogen (N 2) fixation have been studied throughout the growth period with N 2 fixation activity assessed each week by acetylene

Finale

Line 776 Flowering to initiation of seed filling (ISF) Flowering

Flowering 0.4

~

°t 0,nlllIIHlnn

0.2

o,..~r~....u

"0.I ,~L1 I "0.2 4"

3

5

ft. .u u, .u .u .B.u .u .u .u u. u. u. u. t. - -,

7

8

11 13 15 =17= 19 "21' =23

0"5 I 0.3 0.2 0.1 0

. . . . . . . . . .

- . . . . . .

"-~ - . 5. ~J . .7 . .9"

.0.1 b "

/

11" ,13. .15.

. 17. . 19. . 21 . . 23 . . 25 . . 27 . . 29 . . .31. .33. .3S. . 37.

-0.2 ,Ik.

Initiation of seed filling (ISF) to 200 degree-days after ISF

~

0.5, 0.4, 0.3, 0,2,

~

0.1,

~

o

0.4 0.3 0.2

_n.,,nnnrln_n ;;

j' '; '5"VLJl.4Ut/t~ ',; ;; ',; ,=l ~J 25

.

.

.

3 v

.

.

.

'

.

,

"-

•

"'-n' ~

~

2~ , .~~ ~s . 27 ~ ~, ~ ~"". ; .

-o12

-0.2

200 degree-days after ISF to physiological maturity 0.5,

0.4 0.3

0.4 0.3 0.2

0.1 D

0.

o

-

-0.1

-0.1

-0.2,

-0,2 4 .

Internodes

, .... 3

5

,r"; ;-:" . . . . . . . . . . . . . . . . . . 7

9

11 13~15

FI-J'lr'IPA'I,, I' '33' '35~ =37' "

Internodes

Fig. 4. Variationof dry matter at different nodes between two successivestages. (Atta, 1995).

R. Cousin~Field Crops Research 53 (1997) 111-130

116 nitrogen fixation activity

~= i.l moles m=/h

~ r 5.95

~,,,,,

i

~ . u

565

....

CE3 Colmo

....

Rnme

/

:

/

i

--

3"

42

49

,56

63

70

77

84

91

Number of days after sowing

Fig. 5. Evolution of nitrogen fixation for different pea lines: the duration of fixation is identical for all the varieties, but the intensity differs. The maximum fixation activity may occur at different stages of development(Cousin, 1988). date contributed to a decrease in the fixation period from 66 days to 52 days, irrespective of variety. However, changes in activity over this period seemed

to be dependent on variety. One month after sowing the ARA value increased. It peaked at different times depending on variety. Then it decreased. Thus it is possible to distinguish between early fixation and late fixation varieties. Early fixation was independent of early flowering. (Fig. 5) (Cousin, 1988). Thus, for some varieties, nitrogen fixation remains efficient during the seed filling of the first fertile nodes. The sequential development of seeds showed that the lower nodes, which had a higher protein content, were formed during nitrogen fixation. Thus, the proteins of these seeds originate from both nitrogen fixation and nitrogen remobilization from vegetative parts of the plant. However the upper seeds of the plant, formed when nitrogen fixation has ceased, were filled only by remobilization. (Figs. 6 and 7) (Atta et al., 1995). The maximum ARA and cumulative ARA values were also a varietal characteristic together with analysis over several years indicating large differences in cumulative ARA values between varieties. For example, in 1991 at Versailles, cumulative ARA values ranged from 2000/x mol. of C 2 H 2 / h / p l a n t for line 776 to 4000 /x mol for the variety Finale (Fig. 8) (Cousin et al., 1992a). Moreover, cumulative ARA values were also correlated with biomass production.

----ARA ° Flowering • initiation seed filling • Physiological maturity ° Protein content ~

60

50

350 == .*

300

250 40 200 30 150

~Z 20 v <

100 10

03

50

0 300

! 500

I 700

I 900

11 O0

I 1300

I 1500

0 1700

Cumulative degree days from sowing Fig. 6. Sequential development of seeds along the main stem. Line 833. The seeds filled during nitrogen fixation (1) had greater protein concentration than those filled when nitrogen fixation ceased (2). (Atta et al., 1995).

117

R. Cousin/Field Crops Research 53 (1997) 111-130 ~ARA • Rowering = Initiation of seed filling • Physiological maturity e Seed protein content

60

#-.

50

7= "8

40

350 * *****

300 250 .~ 200

==

30 150

~ 2=

2o loo

10

50

0 300

I 500

I 700

I 900

I 1100

I 1300

I 1500

0 1700

Cumulative degree days from sowing

Fig. 7. Sequential developmentof seed along nodes of the main stem. Line 776. All seeds were formed when nitrogen fixation ceased. No variation in seed protein content amongnodes of the plant was recorded. (Atta, 1995).

2.5. Seed characteristics

2.5.1. Starch

Starch is the main component of the pea seed, but occurs in several forms (Fig. 9). Smooth-seeded varieties have round starch granules, whereas most of those varieties with wrinkled-seed have composite granules. This character is controlled by a single gene R-r. Some wrinkled seeded varieties had round starch granules, controlled by the gene Rb-rb. The

7000 • 6000. ~

5000, 4000.

"~ 3000.

1991

I Finale --~,.~Frisson -- "~-- Solara 0 ~M &8 765

2.5.2. Protein I

~

e

- - - -a,

20001000~, 400

I 600

double recessive r-rb also had composite granules. Every group has a clearly defined starch content as well as amylopectin and amylose composition (Fig. 10) (Cousin, 1992). These genes also controlled other seed components: including the soluble sugars present, protein content and protein fractions (vicilin, legumin). More recently, Wang and Hedley (1993) obtain several mutants corresponding to three new loci rug3, rug-4 and rug-5. These mutants also affect the starch content and composition of the seed (Hedley et al., 1995).

I 800

I 1000

I 1200

I

1400

Cumulative degree days from sowing

Fig. 8. Cumulated ARA values for different varieties and lines. Versailles, 1991.

Each of the four groups referred to above exhibited genetic variability in protein content. Protein contents ranging from 26 to 33% for wrinkled-seeded varieties, and from 23 to 31% for smooth-seeded varieties. This difference was due to variations in the synthesis of starch, with smooth-seeded group having a higher starch and amylopectin content than wrinkled seeded types. Analysis of diallel crosses showed that the high protein contents depended on recessive genes (Cousin, 1983).

118

R. Cousin/Field Crops Research 53 (1997) 111-130

Fig. 9. Different shapes of starch granules: (a) Round starch granules of the smooth seeded varieties (e.g. Aldot). (b) Composite starch granules of the wrinkled seeded varieties (e.g. Kelvedon Wonder). (c) Round starch granules of some wrinkled seeded varieties (e.g. Alaska Sweet). (d) Composite starch granules of the double recessive line (from Kelvedon Wonder X Alaska Sweet cross).

Experiments carried out in three different locations demonstrate that both genetic and environmental effects are significant (Table 2). Protein content is

different in each group: the lowest in smooth, the highest in double recessive (r-rb). Moreover the vicilin/legumin ratio seems higher for wrinkled seed

100. 90. 80.

70. 60. 50. 40. 30. 20, 10. O,

I

R-Rb ==Proteins

r-Rb oAmylopectin

I

R-rb IAmylose

Fig. 10. Pea seed composition.

r-rb 0Soluble sugars

R. Cousin~Field Crops Research 53 (1997) 111-130

119

Table 2 Variability and variation of protein content. (Cousin et al,, 1992b) Me~s

Me~

26.92 26.16 25.77 25.68 26,05 25.58 26.05 26.26 25.86

26.77 26.33 26.21 26.06 27.06 25.69 26.60 27.20 26.39

26.48

26.21 26.21

25.99 25.45

26.35 25.90

28.34 27.87 29.85 29.45

27.41 27.56 29.17 28.66

27.50 27.33 27.94 28.31

27.75 27.59 28.99 28.81

667 Alaska Sweet Cennia

30.20 28.62 28.67

29.33 28.83 28.19

29.51 28.28 27.45

29.68 28.58 28.11

28.79

831

31.95

30.75

29.08

30.59

30.59

27.85

27.45

26.90

27.40

Pea type

Varieties

Locations Versailles

Mons

Dijon

Smooth-seeded varieties

776 744 Solara Amac Frisson Madria Finale Colmo Amino

26.84 26.50 26.73 26.32 27.98 25.83 26.82 27.86 26.49

26.55 26.31 26.12 26.17 27.14 25.67 26.95 27.48 26.83

Progreta Countess

26.84 26.05

Micro Stampede Mini Alfi

Particular smooth-seeded varieties

Wrinkled-seeded varieties (ra/ra)

Wrinkled-seeded varieties (rb/rb)

Wrinkled-seeded varieties (ra r b / r a rb) Mean

varieties than for smooth ones. An intermediate value is noted for R-rb type (line 667) (Fig. 11). This ratio increases under environmental effects when the protein content decreases, especially for wrinkled seeded varieties et al. (Cousin et al., 1992b).

The four groups previously described (R-Rb, r Rb, R rb, r rb) show an increasing total soluble sugar content and differences in soluble sugar composition. For example, the R-rb group is particularly rich in

• D

[]

~

DD

] 22.00

•

•n

¢ o

o

[]

I 24.00

¢

ab

I ee•~ 0.5 20.00

[]

o

¢ oo

1.5

28.28

2.5.3. Soluble sugars

2.5

o

26.12

•

I

26.00

A•

I 28.00

I 30.00

I 32.00

I 34.00

Protein content (% D.M.)

[[] Frogel • Mini o 667 • Progreta o 776 • Finale] Fig, 11. Variability and variation of Vicilin'/Legumin ratio according to protein content (Cousin et al., 1992b).

R. Cousin/Field CropsResearch 53 (1997) 111-130

120

Table 3 Variability of sugar composition (percent of total dry matter). (Analyses effectuated by Quemener INRA, Nantes) Variety Sugar Total Sucrose Raffinose Stachyose Verbascose Madria Amac Amino Frisson 776 744 Finale Solara

2.2 1.8 2.4 2.2 2.3 2.4 2.2 2.4

0.7 0.6 0.5 0.5 0.8 0.8 0.7 0.8

2.2 1.8 1.7 1.7 2.3 2.6 2.3 2.4

1.9 2.9 2.7 3.0 2.1 1.8 2.1 2.0

7.0 7.1 7.3 7.4 7.5 7.6 7.3 7.6

Micro Stampede Mini Alfi

4.7 3.8 4.6 4.5

1.0 1.1 0.6 0.8

2.8 3.1 2.8 2.4

3.9 4.0 5.2 4.2

12.4 12.0 13.2 11.9

Alaska Sweet 3.0 667 2.8 Cennia 3.3

0.9 0.9 1.2

4.2 3.4 3.1

6.1 6.1 4.4

14.2 13.2 12.0

Progreta Countess 831

0.7 0.8 1.7

1.9 2.4 4.9

2.9 2.1 6.4

8.9 8.8 17.6

3.4 3.5 4.6

verbascose and stachyose. The sucrose content is lowest in smooth seeds (Table 3).

2.5.4. Trypsin inhibitors In Pisum sativum, trypsin inhibitor activity, though relatively low, ranges from 2 to 15 T U I / m g dry matter among varieties (Table 4) (Cousin et al., 1993a; Leterme et al., 1993). Most spring pea varieties with smooth or wrinkled seeds have a low ( 2 - 5 T U I / m g dry matter) TIA. However, some varieties have T I A as high as l 0 units. These varieties contain other type o f starch controlled by r b r b gene (e.g. Alaska sweet 667) or derive from Maro group (e.g. Maro, Progreta, Heron). Winter pea lines selected from crosses between spring pea varieties and wild types, usually exhibit high ( 5 - 1 5 TUI mg dry weight TIA) activity, not related to seed coat characteristics. This originates from the Champagne field pea variety with improved for cold resistance. Pisum abyssinicum also has a high T I A (9,5) (Cousin et al., 1993b). As many winter peas have a high TIA, we initiated a study o f this character. A low activity spring pea variety: Finale was crossed with a high trypsin

inhibitor winter pea variety: Frimas. One hundred F 3 lines were analyzed and segregated in a 1:2:1 ratio. The first group with T I A lower than 6 units activity was controlled by a recessive major gene. The high activity of Alaska Sweet seems also controlled by a single gene linked to r b. Lines r b obtained from Alaska sweet r b after five back-crosses with Aldot R b show the same T I A level as Alaska sweet (Cousin et al., 1993b).

3. Limitations to yield 3.1. Disease resistance Variation in pea yield is often associated with disease. Major diseases of this crop include: fungi - - Ascochyta, Powdery mildew, Downy mildew, Fusarium, Root rot virus - - Pea c o m m o n Mosaic, Pea Enation Mosaic, Pea seed-borne Mosaic, Top yellow • b a c t e r i a - Pseudomonas. Fortunately these diseases require particular and specific environmental conditions, and so vary in incidence with growing area and varietal susceptibilities. Some of them cause severe and others light damage. Many efforts have been made to introduce genetic resistance to diseases (Bernier et al., 1988).

3.1.1. Ascochyta blight W a r k (1950) found that Austrian winter pea exhibited better resistance to Ascochyta pisi than 312 pea lines studied in Australia. Resistance was attributed to three dominant genes. Lyall and Wallen (1958) concluded that resistance in the A100 line was controlled by duplicate dominant genes. Cousin (1974) mentions that Rondo presents a resistance which is controlled by a major gene whose dominance is incomplete and may be modified by some other genes. W h i l e Darby et al. (1985) also mentions resistant lines due to single dominant gene. Cousin et al. (1985) selected lines resistant to different physiological races of A. pisi (Table 5). The resistance found in the variety Rondo was effective against nearly all physiological races of A. pisi and showed good heritability. Some races overcoming the resistance in Rondo. New resistant lines to these races

R. Cousin/Field Crops Research 53 (1997) 111-130

121

Table 4 Trypsin inhibiting activities of some pea varieties Pea Type

Smooth Seed

Wrinkled Seed

Varieties

Trypsin Inhibitor ( T U I / m g DM)

Varieties

Trypsin Inhibitor ( T U I / m g DM)

Roi des fins verts Finale Amino Solara Miranda Colmo Baccara Allround Radley Baroness Chantal Heron Maro Progreta

2.6 2.9-3.6 3.7 -4.1 2 3.7-4 4.2-5.3 3.3-3.6 4.2 10.5 - 11.1 9.4-10.6 7.6-9.0 8.6-10.3 6.2-10.6 7.0-9.6

Lincoln Tezieride Victory freezer

2.7-3.1 3.7 2.8

Alaska sweet 667

7.1 7.3

Pisumabyssinicum

L 808 JI 227

12.8-13.2 13.5-14.5

Winter type

Frimas Frisson Vendevil Midiver Printiver Frilene Amac Rafale Frijaune Mistral Brevent Triolo Booster

8.2 - 12 9.0-15 6.7-8.6 6.6-7.1 8.5 7.9-9.7 6.8-8.2 8.1-9.8 8.3-12.7 11.0-11.4 3.9-5.3 2.8-3.4 2.8-3.7

Frogel

5.7-9.4

Spring type

A. pisi, s e v e r a l r a c e s e x i s t a c c o r d i n g to a r e a s

have been identified in this study including: Kelve-

With

don wonder

b u t it s e e m s t h a t it is p o s s i b l e to s e l e c t r e s i s t a n t l i n e s .

logical

races

and Gullivert. Thus we can list physiodistinguishable

by

differential

hosts.

This resistance seems stable.

Table 5 Physiological races of Ascochytapisi and differential hosts (Cousin et al., 1985) Physiological races (Dr Hubbeling) Name of strain

D No. 1

-Several strains (12)

-No. 4

-No. 14

C Tezier

B --

E --

Gullivert Rondo Finale Kelvedon wonder Dark-skinned perfection Arabal, Cobri, Starcovert, Supcovert, Vitalis

R R R R S S

R R R S S S

R S S S S S

R VLS LS S S S

S R R S S S

R R

R S

R R S

R S S

R = resistant; S = susceptible; VLS = very little susceptibility; LS = little susceptibility.

R. Cousin/Field Crops Research 53 (1997) 111-130

122 In

contrast,

breeding

for

resistance

to

My-

cosphaerella pinodes has been unsuccessful. Ali et al. (1978), in Australia, mention resistance of some lines to strains o f M. pinodes. However, these lines are infected by strains isolated in France (Cousin et al., 1992c). In France, several thousand lines were tested for their susceptibility to this disease. Only a few lines show light symptoms.

3.1.2. Downy mildew D o w n y mildew caused by Peronospora viciae. appears when the weather is cold (below 14°C) and wet, and may be severe in U.K., Netherlands, Sweden, France, New Zealand and Northwestern USA. White and Raphael (1944) reported that a few pea cultivars were resistant under the growing conditions of Tasmania. Dixon (1981) indicated that some varieties show light symptoms. Cousin (1974) shows that some varieties (Cobri, Starnain, Starcovert, Clause 50) are resistant and that this resistance is controlled by a single recessive gene. This resistance seems to belong to the hypersensitivity type.

3.1.3. Powdery mildew Powdery mildew, caused by Erysiphe polygoni is significant wherever peas are grown. It is especially troublesome in environments with warm dry days and cool nights. Resistance to powdery mildew was reported by Harland (1948) in Peruvian peas, and by Pierce (1948) in a selection from Stratagem. This resistance

is controlled by a single recessive gene. Cousin (1965a) studied the reaction of about 400 pea cultivars to E. polygoni and found that some lines of Mexican and Peruvian peas were nearly immune and Stratagem lightly symptoms. This resistance is also controlled by a single recessive gene. It seems that the difference in behavior of Mexican lines and Stratagem is related to different alleles at the same locus. In France, this resistance has been stable since 1965.

3.1.4. Fusarium wilt Pea wilt is caused by several races of Fusarium oxysporum f.sp. pisi, occur mainly in North America, the Netherlands and Belgium. This fungus has a large genetic variability, with race 1 the oldest, the most widely distributed and the most aggressive. Resistance to this race is controlled by a single dominant gene. Then Fusarium oxysporum f.sp. pisi race 2 appeared and caused near wilt (Snyder and Walker, 1935). Another source of resistance controlled by a single dominant gene discovered by Hare et al. (1949) again allowed breeding resistance to near wilt then released the Delwiche C o m m a n d o variety resistant to wilt and near wilt. Hagedorn (1953) obtained the canning pea cultivar New Era. Race 3 (Schreuder, 1951), and race 4 (Bolton et al., 1966) appeared. A new variety, New Wales, was selected which is resistant to the three races 1 - 2 and 4. N o w most pea cultivars are resistant to wilt and this disease may be considered of

Table 6 Physiological races of F. oxysporum f. sp pisi and differential hosts. (Cousin et al., 1985).

Onward Wisconsin perfection Dark skin perfection Delwiche commando New era New Wales Lines (Kraft, Haglund) R: resistant. S: susceptible to wilt. s: susceptible to near wilt. O: no information.

Race 1 Lindford 1928

Race 2 Snyder and Walter 1935

Race 3 Schreuder 1951

Race 4 Buxton 1955

Race 5 Bolton 1966

Race 6 Haglund 1970

S R R R R R R

s s s R R R R

s s O s O O O

s s O s s O R

S S O O S R R

S O O O S S R

R. Cousin~Field Crops Research 53 (1997) 111-130

minor importance. However, the disease remains an important problem in areas where pea is not grown in sufficiently long crop rotations. This is the case in north-western Washington (USA) where pea crops sometimes are grown every two years in the same field. In these conditions, races 5 and 6 appeared (Haglund and Kraft, 1970) which oblige plant breeders to undertake a large program of selection against this disease. Kraft and Haglund (1978) have developed lines resistant to races 5 and 6 (Table 6). 3.1.5. Pea mosaic

Pea mosaic is caused by Bean virus 2 (BV2), Bean yellow mosaic virus (BYMV), or Pea common mosaic virus (PCMV). This disease is of minor importance. Symptoms vary according to the strains. Generally, Pea common mosaic virus strains show a typical mosaic with clear and dark green areas without deformation of the leaves. With Bean yellow mosaic virus strains, the mosaic is more diffuse. Some strains cause vein necrosis and wilt. This disease is aphid-borne. Legumes such as clover and alfafa are reservoirs. Winter pea varieties which are less visited by aphids than spring pea varieties are not infected. Hagedorn (1951) reported that several varieties of the Perfection type were resistant to BYMV, Yen and Fry (1956) and Johnson and Hagedorn (1958) showed that the resistance to BYMV in pea is controlled by a single recessive gene. Cousin (1965b) reported that the resistance to PCMV in pea is also controlled by a single recessive gene. Barton et al. (1964) demonstrated that resistances to BV2 and PCMV are conditioned by the same gene. Cross-protection tests between PCMV and BYMV strains show a cross protection which indicates that these two strains belong to the same virus. Many varieties possess this resistance which is stable. Since 1951, no strain has been identified that could break down this resistance. 3.1.6. Pea enation mosaic

Pea Enation mosaic disease is caused by Pea enation mosaic virus (PEMV) also named virus 1. This virus produces characteristic blister-like ridges called 'enations' on the underside of leaves. The first symptom is vein cleating appearing on recently de-

123

veloped leaflets, then mosaic with translucent spots. Finally, stem, foliage and pods are distorted. Schroeder and Barton (1958) obtained tolerance but not immunity to PEMV by selection of G21 and G168 from PI 140295. This resistance, controlled by a single dominant gene, has not been commonly used by plant breeders, since its use might result in the selection of more aggressive strains. 3.1.7. Pea top yellow

The Top yellow disease of pea is caused by the Pea leafroll virus (PLRV) (syn. Bean leaf roll virus) in Europe and the USA. The symptoms are severe plant stunting, chlorosis of the upper foliage and leaf roll. Hubbeling (1956) found that several cultivars were resistant and Drijfhout (1968) reported that resistance was controlled by a single recessive gene. This resistance is stable. 3.1.8. Pea seed-borne mosaic

A seed-borne mosaic virus disease of pea was observed in the USA for the first time in 1968. Slight mosaic and leaf curling are the characteristic symptoms. Severe reduction in yield has been observed in the field in USA (Kraft and Hampton, 1980). This viral disease is the most widely spread and the most important in the world, because it is transmitted by seed. Stevenson and Hagedorn (1971) discovered resistance in P.I. 193586 and 193835. Hagedorn and Gritton (1973) reported that resistance to PSbMV is controlled by a single recessive gene. At Versailles, the resistance to PSbMV seems to be stable, but other strains have been already detected and other sources of resistance found. The sbm 2 and sbm 3 genes confer resistance to lentil strain PSbMV-L and sbm 4 to PSbMV-P4. The sbm 1, sbm 3 and sbm 4 genes belong to a cluster located on chromosome VI while sbm 2 is linked to the gene mo on chromosome II. The chromosome-6 cluster includes the sbm-1, sbm-3 and sbm-4 genes as well as the cyv-2 gene for resistance to clover yellow vein virus (CYVV) (Provvidenti and Muehlbauer, 1990). The chromosome-2 cluster includes sbm-2, cyv for resistance to CYVV, and mo for resistance to been yellow mosaic virus, as well as genes conferring resistance to others potyviruses (Provvidenti, 1990). The resistance gene-

124

R. Cousin/Field Crops Research 53 (1997) 111-130

cluster containing sbm-1 has been assigned to chromosome-6 as a result o f linkage studies using a number o f chromosome-6 morphological and allozyme markers including wlo (Gritton and Hagedorn, 1975) and Prx-3 ( W e e d e n et al., 1991). Recently, the nucleotide sequence and deduced amino acid sequence of pathotype P-4 were determinated and compared to the corresponding sequences of pathotype P-1 (Johansen et al., 1996).

3.1.9. Pea early browning virus This disease is known in the north o f Europe: England and the Netherlands. Veins of stipules and leaflets become necrotic and localized wilting appears. Symptoms may be restricted to a few leaves or a portion o f the leaves or stipules. Pods show a purple-brown necrotic pattern. This virus might be transmitted by the nematodes Trichodorus teres (Van Hoof, 1962). 3.1.10. Bacterial blight Bacterial blight is caused by Pseudomonas syringae pv. pisi. This disease appears in particular on winter peas. But it can also occur on spring peas. P. syringae pv. pisi was isolated from 20% of the field pea crops sampled in the W i m m e r a region of Victoria, Australia (Hollaway and Bretag, 1995). In U.K. the incidence of infection, across all categories o f seed tested has highly increased over the last eight years from 8.2% infected to 36.5%. Race 2 o f the pathogen was most frequently isolated from infected seed samples and often associated with race 6 (Reeves et al., 1996). N o w seven physiological races are known. In 1993, a source o f resistance to race 6 was found by R. Cousin and J. Schmit in France and J. Taylor in England in some lines o f Pisum abyssinicum (Cousin et al., 1995; Schmit et al., 1993). Thus, we now have all the differential hosts with which to identify physiological races (Table 7). The segregation analyses of F 3 lines from crosses between differential hosts have enabled the genetic study of specific resistances. The resistances to race 1 and race 2 studied in the Lincoln × Early Onward and Lincoln × Partridge crosses are controlled respectively by single dominant genes. Resistances to race 3 and race 4 studied in the Lincoln × A b a d o r and Lincoln × Progreta crosses are controlled respec-

Table 7 Physiological races of Pseudomonas syringae and differential hosts Race1 Race2 Race3 Race4 Race5 Race6 Lincoln Progreta Abador Partridge Belinda Early onward P.abyssinicum

R R R R R S R

R R R S S R R

R R S R R S R

R S R R S S R

R R R R S R R

S S S S S S R

tively by single recessive genes. F r o m the Lincoln × Belinda cross, the resistance to race 5 was found to be controlled by a single recessive gene. The dominant gene which gives resistance to race 2 also confers resistance to race 5. The recessive gene which gives resistance to race 3, also confers resistance to race 1. Finally, the resistance to race 6 in Pisum abyssinicum is also controlled by another recessive gene (Cousin et al., 1995).

3.1.11. Molecular markers In order to facilitate breeding for disease resistance, research for molecular markers linked to resistant genes has been carried out (Dirlewanger et al., 1994). R L F P markers p252, p254, p248, p227, p105, p236 and R A P D markers H19, Y14, Y I 5 are found linked to resistance genes mo, Fw, er. Some QTL I

IV

II

VI

- - p236

.H19

14.4

15.9 I

6.2

• . Y14

9.B

er

9.4

I p252

• '

FW

6.0

• ~p254 4 . 0 . p248

30.0

13.7

I

QTL concerning Ascochytablight

Y15 !

12"51 105

sbm-1 sbm-3 sbm-4

3227

Fig. 12. Partial genetic linkage map of pea constructed with MAPMAKER. Resistance genes and markers are on the right side of the chromosome and distances given in cM are on the left. (Didewanger et al., 1994).

R. Cousin/Field Crops Research 53 (1997) 111-130

were also mapped for resistance to Ascochyta pisi race c (Fig. 12). In the same way Timmerman et al. (1994) identified a RAPD marker (PD10650) tightly linked to powdery mildew resistant gene: er, and the RFLP marker GS185 closely linked to sbm-1 (Timmerman et al., 1993).

3.2. Environmental stress tolerance The improvement of yield stability in many grain legume species and especially in dry pea is a major breeding objective. Cold and drought are the most important environmental stresses.

3.2.1. Cold resistance The performance of the many pea cultivars is considerably affected by cold. Most lines and cultivars are very susceptible to cold, especially early lines or lines with long internodes, large leaf area or wrinkled seeds. Only a few lines from wild Pisum species or forage winter pea, probably originating

3.1.12. Transformation Transformation in legume is especially difficult. However, some transformants have been obtained by Schroeder et al. (1993) and more recently by Grant et al. (1995). However the application of this technique remains problematic.

• Fodderpea parental8enotypes D Winter pea parentalgenotypes • Springpea parentalgenotypes

•••e•devil

lOO /

/ / ~BCam/~//~

7

~

o

125

~ Champagne r~/~ Austrianwinter ~D~ Frisson wink°ssa

ivil

Colmo

i

0

5O

100

Variance (Vr)

2OO

Vendevilt2 :Champagne 150

+

>-

FrissonD

/ / /

Austrian winter

100

c 50

/I Pilet

/ Merlivil BIB • Finale. Colmo

o 0

1000 2 0 0' 0 30 0o Temperature (-*C) x Time (hours)

Fig. 13. Level o f cold resistance in diallel crosses in pea, i n v o l v i n g fodder, winter or spring p e a parental genotypes.

R. Cousin/Field Crops Research 53 (1997) 111-130

126

2.0

Specific combining ability with winter cullivars: •

Frisson

zx Vendevil

.~

t ttt

1.5

.N

•

Winkossa C

1.0

e,,¢

.0

El General combining

ability of spring cultivars

E

8 (a

l

0.5

0.0

-0.5 I

I

I

I

I

1

.~.~ E,~ _-~ -

g

I

~

I

I

°

I

~

I

I

I

I

I

I

I

~-.~-~'~

-~

I ....

I

I

~ ~ ~

~-

-=

Spring cultivars Fig. 14. Specificcombiningability and general combiningability for 20 spring cultivars and three winter cultivars.

from P. a r v e n s e are very resistant to cold: These include Champagne and Haute-Loire from France, Fenn and Melrose from the USA and Austrian winter from Austria. Winter hardiness in the P i s u m species is reported to be a quantitatively inherited trait (Auld et al., 1983; Cousin, 1983; Markarian and Andersen, 1966). The study of the progeny of crosses between spring peas and Champagne or Haute-Loire showed that it is possible to transfer cold resistance from the fodder winter pea to vining or combining peas. The analysis of diallel crosses showed that cold resistance is a quantitative character, with intermediate dominance. All lines are distributed along a regression line of slope 1 (b = 1) above the first bisector. The parental genotypes of winter fodder pea lines seem to possess more recessive genes for cold resistance than winter and spring lines (Fig. 13). In the progeny of some crosses, it is possible to obtain transgressive segregants for this character, and thus from the Frimas x Floriver progeny, lines with greater cold resistance than their parents were selected. The quantitative character for cold resistance having been demonstrated, recurrent selection was un-

dertaken. First, we looked for high combining ability between spring and winter cultivars (Fig. 14). Then cultivars which showed a high general combining ability were intercrossed, using a circular crossing scheme in order to bring together the most cold resistance genes (Fig. 15). Lastly, progenies were selected under field conditions and under controlled conditions (Cousin et al., 1993c). In order to assess cold resistance, a selection method under controlled conditions was developed Mihan

Anik

swa°99'°°l

Winkossa

Frisson

Hativer

Fig. 15. Circular crossing scheme used to breed pea cultivars with high levels of cold resistance.

R. Cousin~Field Crops Research 53 (1997) 111-130

by Prieur and Cousin (1978). Before exposing plants to the required minimum temperature, we subjected them to a progressive decrease in temperature over a period of 2 - 3 weeks so that they became hardened. After the plants had been subjected to below-zero temperatures, for varying periods, the temperature was gradually increased. This method makes easier the classification of different lines according to their degree of cold resistance. Several characters seem to be associated with winter hardiness. Pigmented hilums conditioned by a dominant gene, Pl, on chromosome VI were strongly associated with winter hardiness Liesenfeld et al. (1986); Markarian and Andersen (1966). Pigmented seed coats and yellow cotyledons, conditioned by the dominant genes A and I, respectively, on chromosome 1, were associated with cold resistance. Murray et al. (1988). Powdery mildew resistance conditioned by the recessive gene er on chromosome V1 seems to be linked to the major susceptible gene (D.L. Auld, personal communication). The same linkage has been noted for greater amounts of trypsin inhibitors in seeds, but, in many cases, these linkages have been broken.

3.2.2. Drought tolerance Drought stop the nitrogen fixation and decreases the biomass production (Cousin et al., 1993c). Biarnes Dumoulin et al. (1996) in a study of 10 genotypes sown at two dates during two years at three locations in France confirmed the existence of high variability for yield. The environmental effect was preponderant and essentially due to differences of soil water availability during the flowering period. The genotype × environment interaction is determined by the differential response of genotypes, according to their earliness to flower and the duration of the seed set period, when grown under drought stress conditions during the sensitive flowering period.

4. Conclusion Dried peas give high yields potentially reaching 8 tons per hectare. However, many biotic or abiotic factors limit this production. The ideal pea plant is well established and selection traits have been deter-

127

mined. The use of the afila gene has contributed to a decrease in leaf area and an increase in yield. Resistance to lodging remains to be improved. The number of fertile nodes must be reduced, perhaps by introducing genes that determine plant growth. Assimilation and nitrogen fixation are well understood. However, factors limiting seed filling in some varieties or those reducing the nitrogen remobilization from leaves to seeds when the biomass production is high, remain to be found. Cold and disease resistance have been greatly improved. However new improvements remain possible as the selected winter pea cultivars are still less resistant to cold than resistant wild pea germplasms. Effective resistance to Ascochyta blight caused by Mycosphaerella pinodes, root rot caused by Aphanomyces euteiches, or pea enation mosaic virus, remains elusive. In these cases classical breeding by vertical gene management cannot be undertaken. Finding polygenic resistance or transferring artificial resistance genes should be investigated. Research concerning pea transformation needs to be increased. This should, for example, allow the introduction into peas of resistances to insects, viruses or herbicides against which there is no natural resistance. Wide variability exists for seed constituents in peas. Peas constitute an important source for feed and food manufacturers. The range of different uses of peas could be increased. Breeding for varieties with very thick edible pod could be considered a good strategy for finding a new vegetable. Research for increasing amylose content in pea seeds may also be a strategy for obtaining the new biodegradable plastic materials used by car manufacturers.

References Ali, S.M., Nitschke, L.F., Dube, A.J., Krause, M.R. and Cameron, B., 1978. Selection of pea lines for resistance to pathotypes of

Ascochyta pinodes, A. pisi and Phoma medicagenis vat. pinodella, Austral. J. Agric. Res., 29: 841-849. Atta, S., Maltese, S. and Cousin, R., 1995. Influence of nitrogen fixation on seed protein content in pea (Pisum sativum L.). 2nd European Conf. on Grain Legumes, Copenhagen, 9-13 July 1995, AEP, Paris, p. 417. Atta, S., 1995. Etude de la variabilit6 grnrtique pour la fixation et la remobilisation de l'azote chez le pois (Pisum sativum L.).

128

R. Cousin~Field Crops Research 53 (1997) 111-130

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