Field

Crops _
ELSEVIER
Research
Field Crops Research 53 (1997) 111-130

Peas ( Pisum sativum L.)

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

1. Introduction 2. Origin and general botany

Peas have been grown as an important source of

The pea has been known since antiquity.
animal feed and human food for many centuries.
Theophrastus (1961), in his book Enquiry into plants
Over this time, pea has been selected for these uses.
translated in English by Arthur Hort, mentions traces
Several thousand varieties exist throughout the world.
of pea much earlier than 300 years B.C. He describes
They can be classified into the following categories:
several species of legumes and especially the 'Pea'
• field peas, providing forage for animal feed;
and reveals that peas were used for fodder and
• market peas, from which pods are harvested for
human food.
human consumption as a fresh vegetable;
The pea crop was known in the prehistoric age in
• vining peas, for canning or freezing;
Europe. Peas dating from the Stone Age have been
• dried peas, partly for human consumption but
discovered in the excavations at Aggetelek in Hun-
mostly for animal feed.
gary and in lake-dwellings in Switzerland (Four-
Considerable developments have been made with
mont, 1956). In France, peas exhumed from dwellings
dried peas over the last decade in order to further
in the Bourget lake belong to the Bronze Age,
satisfy the needs concerning animal feed.
(1000-2000 B.C.) and are assumed to have been
World production of dried peas is currently esti-
grown by Aryan people (Gibault, 1912). Recently,
mated to be 16 million tons. The primary areas of
Smartt (1990) in his book Grain Legumes: Evolution
production are the former USSR (7.3 MT), Europe
and Genetic Resources, indicates that peas date back
(4.8 MT; of which France produces 3.2 MT) and
to 7000-6000 B.C. Erskine et al. (1994) mentions
China (1.6 MT). The world average yield per hectare
that peas were rare at Jarmo, Iraq (6750 B.C.), while
was 1.82 tons and was greatest in France (4.95 tons
they constitute the prevalent pulse at a Neolithic site
ha -1) and least in India (0.92 tons ha -1) (FAO,
at Erbaba in Turkey (5800-5400 B.C.).
1991).
Peas probably originated in Abyssinia and
However, the yield within different countries was
Afghanistan, with areas in the Mediterranean area
unstable. Consequently, many characters have to be
colonized later. From these areas the pea spread to
improved in order to satisfy the developing needs of
other parts of Europe and Asia. Botanists have de-
growers, processors and feed manufacturers.
scribed 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.
* Corresponding author. abyssinicum, P. aethiopicum, P. arvense; but, most

0378-4290/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved.

PII S0378-4290(97)00026-9
112 R. Cousin/Field Crops Research 53 (1997) 111-130

frequently, they are considered as belonging to the two wings and a keel formed as the result of fusion
Pisum sativum species (Fourmont, 1956). of two petals surrounding ten stamens and one style.
These wild species often have tall, (more than 2 The pea is cleistogamous and must be considered as
meters), slender and branched stems, purple or pink a strictly self-fertilizing species, though Xylocopa
flowers and small pods producing a small quantity of and Megachile do visit pea flowers and can be
seeds with colored coat. P. elatius and P. responsible for natural hybridizations. Thus, some
abyssinicum have distinct toothed leaflets and stip- genetic mixing can take place without the interven-
ules. P. elatius has colored flowers, lilac-blue stan- tion of pea breeders. Natural populations and vari-
dards, dark purple wings and maroon veiny brown eties consist of genetically stable plants.
seeds. P. abyssinicum has pink flowers and dark All cultivated pea varieties are pure lines. In order
purple seeds. P. fulvum may have two fructification to obtain hybrid varieties, it would be necessary to
types, a normal one located in the upper part of the find mutants with open flowers, a male sterile source
plant, the other very peculiar with very short basal and an efficient pollen carrier. Artificial seed produc-
branches which push the pods slightly into the tion might also be considered after micropropagation
ground. P. humile is characterized as a medium of hybrid seeds. But, due to the complexity of these
sized climbing species with dentate leaf margins and techniques and the profitability which is yet to be
light blue flowers. proven, it seems probable that pure line varieties will
The two forms of cultivated pea, the field pea (P. continue to be used.
arvense L.) and the garden pea (P. sativum L.) are
sometimes regarded as separate species. There is 2.2. Yield and plant characteristics
very little justification for this since they can be
crossed readily and are quite inter-fertile. It seems Pea plants exhibit an indeterminate growth habit.
probable that the garden pea was derived by selec- The first nodes, some of which give rise to branches,
tion from the field pea (Smartt, 1976). Based on are vegetative, while subsequent nodes are reproduc-
analyses of morphology, cytogenetics and hybrid tive. Generally two flowers, from which the pods
performance, Ben-Ze'ev and Zohary (1973) con- develop, are present at each reproductive node. The
cluded that P. fulvum is a fully divergent species, number of seeds per pod depends on the variety and
whereas P. humile, P. elatius and P. sativum form a on the environmental conditions.
single species complex. Other researchers show that There is a large genetic variability for number of
Pisum is monospecific, suggesting that the differ- branches, pods, seeds per pod, thousand-seed weight,
ences observed for P. fulvum relative to the other leaf area, height of the plant. However, when crosses
pea taxa are more a matter of degree than the basis are made which attempt to improve on, and combine
for a distinct species (Wellensiek, 1925; Hedrick, these traits, yields are often reduced.
1928; Lamprecht, 1966; Blixt, 1974). Davies (1974), In order to better define the characters limiting
Marx (1977) and Palmer et al. (1985) agree with the yield, yield variations have been studied for a range
conclusion that P. humile is the wild progenitor of of varieties in a progressive multiple regression anal-
the cultivated pea. Recently, Hoey et al. (1996) have ysis involving variations in a range traits. In this
confirmed this origin through a phylogenetic analysis analysis only thousand seed weight, seedling vigor
based on certain morphological characters and RAPD and harvest index were positively correlated with
markers. In the same way Samec and Nasinec (1996), yield, though correlation coefficients were low, while
using also RAPD Technique and dendrogram repre- a number of the traits studied were negatively corre-
sentation, analyze relationships among lines of P. lated with yield (Table 1) (Cousin et al., 1985).
sativum ssp. elatius, P.s. ssp. aruense, P.s. ssp. From this data it appears that when vegetative
humile and P.s. ssp. sativum. growth is vigorous, there is increased interplant com-
petition and yield suffers. Reduction in leaf area and
2.1. Plant biology and controlled pollination
plant height to produce smaller, more highly branched
The pea flower is typical of the Papilionaceae plants and increasing of the thousand seed weight
family. The corolla contains five petals: the standard, 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

Plant
Height - 0.39 b -- 0 . 6 6 b -- 0 . 7 0 b -- 0.35 b -- 0 . 2 4
(Sum heat unit) 2 0.23 - 0.28 - 0.19 - 0.33 b 0.09
Thousand-seed weight 0.24 0.49 b 0.41 b 0.42 b 0.33 b
Number of seeds per pod - 0.01 - 0.04 - 0.02 0.16 - 0.08
Leaf area -0.18 -0.41 b --0.41 b 0.15 --0.11
Seedling vigour (dry matter) 0.27 b 0.44 b --0.10 0.35 b 0.34 b
N u m b e r o f fertile b r a n c h e s 0.19 0.31 0.18
at the top -0.18 -0.34 b
at t h e b o t t o m 0.05 0.29
Harvest index 0.36 b 0.37 b

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 b --0.27 " 0.01 --0.38 b

a 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%.

peas also revealed the necessity of reducing the leaf seed weight. This leads to the concept of reducing
area. But winter peas may be taller, and seed size the biomass in order to increase seed yield.
seems to be less important. Seeds may be smaller
and more numerous. 2.3. Biomass and seed production
Decrease of leaf area is undoubtedly the genetic
improvement which will most improve productivity In order to study the relationships between
and stand. Several genes are available that reduce biomass production and seed yield, the dry matter
leaf area (Fig. 1): has been measured in different organs of the plant
'af' gene converts leaflets to tendrils and gives during plant development. This study, carried out on
'semi-leafless peas'; several varieties, reveals that the genetic variability
'st' gene gives reduced stipules, and combined exists for biomass production and translocation ca-
with the 'af' gene results in leafless peas; pacity.
'Rogue' gene reduces the leaflet and stipule size, For instance, results obtained with eM, Frisson,
and makes them erect like hare's-ears. Finale and 776 show this variability (Fig. 2):
Of these the 'semi-leafless' type appears to be the • eM, very early line, has low biomass, good
most promising. The 'af' gene induces a 40% de- translocation and medium yield;
crease in leaf area, with the leaf area better dis- • Frisson and Finale, intermediate flowering culti-
tributed along the stem, chiefly at the level of the vars, have medium biomass production, better
fertile nodes. This contributes to better light penetra- translocation capacity and higher seed yield;
tion through the canopy. Isogenic lines yield 0 to • 776, late line, has the highest biomass production
20% more than normal foliage lines. These lines also and the lowest translocation capacity. The seed
show better standing ability which facilitates me- yields becomes very low.
chanical harvesting. When biomass production becomes too high, in-
These analyses reveal that it is necessary to re- terplant competition reaches a high level and the
duce most of the yield factors excepted thousand seed yield decreases. Thus the translocation capacity
114 R. Cousin~Field Crops Research 53 (1997) 111-130

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

409 508 564 658 763 899 1001 1169

a b

409 508 564 858 763 829 1001 1169 1255 t370 1485

409 508 564 558 763 899 1001 1189 1255 1370 1485

d • f 4O9 508 564 658 763 899 1001 1166 1255 1370 1485

Fig. 1. Different morphological types of pea leaves. (a) Normal Cumulativedegreedaysfromsowing

leaf. (b) Semi-leafless or 'afila', 'af' gene transforms the leaflets
Fig. 2. Dry matter accumulation in different organs during plant
into tendrils. (c) Leafless, combination of 'af' and 'st' genes. The
development. (Atta, 1995).
'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. 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

may be a determinant factor for yield. Utilization of

15N reveals that the decrease in dry matter of the Line 833 Frlsson
vegetative organs results essentially from the remobi-
lization of nitrogenous substances.

1111
The utilization of 15N applied at different stages
of plant growth, has shown that nitrogen is stored in
temporary organs, then transferred to young struc- ~ ,o
tures of the plant and finally remobilized towards the
2
seeds. Genetic variability exists for the translocation
capacity. The study of two genotypes indicated that i I I I I I
VS FIo. Filfing Maturity VS FIo, Filing Matudty
the remobilization began early and was greater for
'Frisson' than to line 833 (Fig. 3) (Atta, 1995). • Seeds [ ] Lowerleaves [ ] Stems
Differences in remobilization from different nodes
can explain the differences in seed yield between [] Pods [] Upperleaves [ ] Roots
776 and 'Finale'. For the high yielding 'Finale', the Fig. 3. Distribution of 15N in different organs during plant devel-
dry matter was remobilized from all nodes of the opment following labeling at the vegetative stage. (Atta, 1995).
 R. Cousin/ FieM Crops Research 53 (1997) 111-130 115

vegetative growth was not completely over (Fig. 4) reduction activity (ARA) method (Balandreau and
(Atta, 1995). Dommergues, 1973). The duration of the fixation
Biomass production and remobilization are linked period was the same for all varieties, irrespective of
to nitrogen fixation. Thus, it is necessary to know the flowering date. It began one month after sowing and
genetic variability for nitrogen (N 2) fixation. lasted up to two months. Consequently, for an early
2.4. Nitrogen fixation variety, N 2 fixation continued during seed develop-
ment while, for a late variety, it stopped after flower-
Varietal differences in nitrogen (N 2) fixation have ing. Moreover, if sowing was delayed, fixation activ-
been studied throughout the growth period with N 2 ity increased more rapidly while the duration de-
fixation activity assessed each week by acetylene creased. In 1991, a one month delay in the sowing

Finale Line 776

Flowering to initiation of seed filling (ISF)
Flowering
Flowering

0.4
0"5 I

°t 0,nlllIIHlnn
0.3
~ 0.2 0.2

o,..~r~....u
ft.
.u u, .u .u .B.u .u .u .u u. u. u. u. t. - -,
0.1
0 . . . . . . . . . . - . . . . . .
"0.I ,~L1 3 5 7 8 11 13 15 =17= 19 "21' =23
.0.1 b " . .7 . .9"
"-~ - . 5. ~J 11" ,13. .15. . 17. . 19. . 21
. . 23
. . 25
. . 27 . . .31. .33. .3S. . 37.
. . 29
I /
"0.2 4" -0.2 ,Ik.

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

0.5,
0.4, 0.4
0.3, 0.3
~ 0,2, 0.2
~ 0.1, _n.,,nnnrln_n
~ o ;; . . . . . . . , •

j' '; '5"VLJl.4Ut/t~ ',; ;; ',; ,=l ~J 25 3 v ' "- "'-n' ~ ~ , .~~ ~s . 27 ~ ~, ~ ~"". ; .
2~
-0.2 -o12

200 degree-days after ISF to physiological maturity

0.5,

0.4 0.4
0.3 0.3

0.2
0.1 0.
D o - , .... ,r"; ;-:" . . . . . . . . . . . . . . . . . . FI-J'lr'IPA'I,,
-0.1 -0.1 3 5 7 9 11 13~15 I' '33' '35~ =37' "
-0.2, -0,2 4 .

Internodes Internodes
Fig. 4. Variationof dry matter at different nodes between two successivestages. (Atta, 1995).
116 R. Cousin~Field Crops Research 53 (1997) 111-130

nitrogen fixation activity

~= - ~ r to be dependent on variety. One month after sowing
i.l moles m=/h ~,,,,, 5.95
the ARA value increased. It peaked at different times
~ . u 565 depending on variety. Then it decreased. Thus it is
.... CE3
Colmo possible to distinguish between early fixation and
i .... Rnme late fixation varieties. Early fixation was independent
of early flowering. (Fig. 5) (Cousin, 1988).
: / Thus, for some varieties, nitrogen fixation re-
mains efficient during the seed filling of the first
fertile nodes. The sequential development of seeds
/ i showed that the lower nodes, which had a higher
protein content, were formed during nitrogen fixa-
tion. 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 remobiliza-
--
tion. (Figs. 6 and 7) (Atta et al., 1995).
3" 42 49 ,56 63 70 77 84 91 The maximum ARA and cumulative ARA values
Number of days after sowing were also a varietal characteristic together with anal-
Fig. 5. Evolution of nitrogen fixation for different pea lines: the ysis over several years indicating large differences in
duration of fixation is identical for all the varieties, but the cumulative ARA values between varieties. For ex-
intensity differs. The maximum fixation activity may occur at ample, in 1991 at Versailles, cumulative ARA values
different stages of development(Cousin, 1988). 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)
date contributed to a decrease in the fixation period (Cousin et al., 1992a).
from 66 days to 52 days, irrespective of variety. Moreover, cumulative ARA values were also cor-
However, changes in activity over this period seemed related with biomass production.

----ARA
60 ° Flowering 350
• initiation seed filling
• Physiological maturity ==
300
50 ° Protein content ~ .*

250
40

200
30

~Z 150

20
v 100 03

<
10
50

0 ! I I I I 0
300 500 700 900 11 O0 1300 1500 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).
 R. Cousin/Field Crops Research 53 (1997) 111-130 117

60 ~ARA 350
• Rowering
= Initiation of seed filling * *****
• Physiological maturity 300
#-. 50
e Seed protein content
250 .~
7= 40
"8
200
== 30
150 ~
2=
2o
loo

10
50

0 I I I I I I 0
300 500 700 900 1100 1300 1500 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 double recessive r-rb also had composite granules.
Every group has a clearly defined starch content as
well as amylopectin and amylose composition (Fig.
2.5.1. Starch 10) (Cousin, 1992).
Starch is the main component of the pea seed, but These genes also controlled other seed compo-
occurs in several forms (Fig. 9). Smooth-seeded nents: including the soluble sugars present, protein
varieties have round starch granules, whereas most content and protein fractions (vicilin, legumin).
of those varieties with wrinkled-seed have composite More recently, Wang and Hedley (1993) obtain
granules. This character is controlled by a single several mutants corresponding to three new loci rug-
gene R-r. Some wrinkled seeded varieties had round 3, rug-4 and rug-5. These mutants also affect the
starch granules, controlled by the gene Rb-rb. The starch content and composition of the seed (Hedley
et al., 1995).

7000 •
1991
I Finale 2.5.2. Protein
6000.
--~,.~Frisson
Each of the four groups referred to above exhib-
~ 5000, -- "~-- Solara
0 ~M
I ited genetic variability in protein content. Protein
4000.
&8 765 ~ e - - - -a,
contents ranging from 26 to 33% for wrinkled-seeded
"~ 3000. varieties, and from 23 to 31% for smooth-seeded
2000- varieties. This difference was due to variations in the
1000- synthesis of starch, with smooth-seeded group hav-
~, I I I I I
ing a higher starch and amylopectin content than
400 600 800 1000 1200 1400 wrinkled seeded types.
Cumulative degree days from sowing Analysis of diallel crosses showed that the high
Fig. 8. Cumulated ARA values for different varieties and lines. protein contents depended on recessive genes
Versailles, 1991. (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 loca- different in each group: the lowest in smooth, the
tions demonstrate that both genetic and environmen- highest in double recessive (r-rb). Moreover the vi-
tal effects are significant (Table 2). Protein content is cilin/legumin ratio seems higher for wrinkled seed

100.
90.
80.

70.
60.
50.
40.
30.
20,
10.
O, I I
R-Rb r-Rb R-rb r-rb

==Proteins oAmylopectin IAmylose 0Soluble sugars

Fig. 10. Pea seed composition.

 R. Cousin~Field Crops Research 53 (1997) 111-130 119

Table 2
Variability and variation of protein content. (Cousin et al,, 1992b)
Pea type Varieties Locations Me~s Me~
Versailles Mons Dijon
Smooth-seeded varieties 776 26.84 26.55 26.92 26.77
744 26.50 26.31 26.16 26.33
Solara 26.73 26.12 25.77 26.21
Amac 26.32 26.17 25.68 26.06
Frisson 27.98 27.14 26,05 27.06 26.48
Madria 25.83 25.67 25.58 25.69
Finale 26.82 26.95 26.05 26.60
Colmo 27.86 27.48 26.26 27.20
Amino 26.49 26.83 25.86 26.39

Particular smooth-seeded varieties Progreta 26.84 26.21 25.99 26.35

Countess 26.05 26.21 25.45 25.90 26.12

Wrinkled-seeded varieties (ra/ra) Micro 28.34 27.41 27.50 27.75

Stampede 27.87 27.56 27.33 27.59
Mini 29.85 29.17 27.94 28.99 28.28
Alfi 29.45 28.66 28.31 28.81

Wrinkled-seeded varieties (rb/rb) 667 30.20 29.33 29.51 29.68

Alaska Sweet 28.62 28.83 28.28 28.58 28.79
Cennia 28.67 28.19 27.45 28.11

Wrinkled-seeded varieties (ra r b / r a rb) 831 31.95 30.75 29.08 30.59 30.59

Mean 27.85 27.45 26.90 27.40

varieties than for smooth ones. An intermediate value 2.5.3. Soluble sugars
is noted for R-rb type (line 667) (Fig. 11). This ratio The four groups previously described (R-Rb, r
increases under environmental effects when the pro- Rb, R rb, r rb) show an increasing total soluble sugar
tein content decreases, especially for wrinkled seeded content and differences in soluble sugar composition.
varieties et al. (Cousin et al., 1992b). For example, the R-rb group is particularly rich in

2.5
• D [] ~ []
DD •
•n
o ¢ o
oo ¢
o o [] ¢
1.5 ab

I ee•~ • A•

0.5 ] I I I I I I
20.00 22.00 24.00 26.00 28.00 30.00 32.00 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).
120 R. Cousin/Field CropsResearch 53 (1997) 111-130

Table 3 inhibitor winter pea variety: Frimas. One hundred F 3

Variability of sugar composition (percent of total dry matter). lines were analyzed and segregated in a 1:2:1 ratio.
(Analyses effectuated by Quemener INRA, Nantes)
The first group with T I A lower than 6 units activity
Variety Sugar Total was controlled by a recessive major gene.
Sucrose Raffinose Stachyose Verbascose The high activity of Alaska Sweet seems also
Madria 2.2 0.7 2.2 1.9 7.0 controlled by a single gene linked to r b. Lines r b
Amac 1.8 0.6 1.8 2.9 7.1 obtained from Alaska sweet r b after five back-crosses
Amino 2.4 0.5 1.7 2.7 7.3 with Aldot R b show the same T I A level as Alaska
Frisson 2.2 0.5 1.7 3.0 7.4
776 2.3 0.8 2.3 2.1 7.5 sweet (Cousin et al., 1993b).
744 2.4 0.8 2.6 1.8 7.6
Finale 2.2 0.7 2.3 2.1 7.3
Solara 2.4 0.8 2.4 2.0 7.6 3. Limitations to yield
Micro 4.7 1.0 2.8 3.9 12.4
Stampede 3.8 1.1 3.1 4.0 12.0 3.1. Disease resistance
Mini 4.6 0.6 2.8 5.2 13.2
Alfi 4.5 0.8 2.4 4.2 11.9 Variation in pea yield is often associated with
Alaska Sweet 3.0 0.9 4.2 6.1 14.2 disease. Major diseases of this crop include:
667 2.8 0.9 3.4 6.1 13.2 fungi - - Ascochyta, Powdery mildew, Downy
Cennia 3.3 1.2 3.1 4.4 12.0 mildew, Fusarium, Root rot
Progreta 3.4 0.7 1.9 2.9 8.9 virus - - Pea c o m m o n Mosaic, Pea Enation Mo-
Countess 3.5 0.8 2.4 2.1 8.8 saic, Pea seed-borne Mosaic, Top yellow
831 4.6 1.7 4.9 6.4 17.6 • b a c t e r i a - Pseudomonas.
Fortunately these diseases require particular and
specific environmental conditions, and so vary in
verbascose and stachyose. The sucrose content is incidence with growing area and varietal susceptibili-
lowest in smooth seeds (Table 3). ties. Some of them cause severe and others light
damage.
2.5.4. Trypsin inhibitors Many efforts have been made to introduce genetic
In Pisum sativum, trypsin inhibitor activity, resistance to diseases (Bernier et al., 1988).
though relatively low, ranges from 2 to 15 T U I / m g
dry matter among varieties (Table 4) (Cousin et al., 3.1.1. Ascochyta blight
1993a; Leterme et al., 1993). Most spring pea vari- W a r k (1950) found that Austrian winter pea ex-
eties with smooth or wrinkled seeds have a low ( 2 - 5 hibited better resistance to Ascochyta pisi than 312
T U I / m g dry matter) TIA. However, some varieties pea lines studied in Australia. Resistance was at-
have T I A as high as l 0 units. These varieties contain tributed to three dominant genes. Lyall and Wallen
other type o f starch controlled by r b r b gene (e.g. (1958) concluded that resistance in the A100 line
Alaska sweet 667) or derive from Maro group (e.g. was controlled by duplicate dominant genes. Cousin
Maro, Progreta, Heron). (1974) mentions that Rondo presents a resistance
Winter pea lines selected from crosses between which is controlled by a major gene whose domi-
spring pea varieties and wild types, usually exhibit nance is incomplete and may be modified by some
high ( 5 - 1 5 TUI mg dry weight TIA) activity, not other genes. W h i l e Darby et al. (1985) also mentions
related to seed coat characteristics. This originates resistant lines due to single dominant gene. Cousin et
from the Champagne field pea variety with improved al. (1985) selected lines resistant to different physio-
for cold resistance. Pisum abyssinicum also has a logical races of A. pisi (Table 5). The resistance
high T I A (9,5) (Cousin et al., 1993b). found in the variety Rondo was effective against
As many winter peas have a high TIA, we initi- nearly all physiological races of A. pisi and showed
ated a study o f this character. A low activity spring good heritability. Some races overcoming the resis-
pea variety: Finale was crossed with a high trypsin tance 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 Varieties Trypsin Inhibitor
( T U I / m g DM) ( T U I / m g DM)
Spring type Roi des fins verts 2.6 Lincoln 2.7-3.1
Finale 2.9-3.6 Tezieride 3.7
Amino 3.7 -4.1 Victory freezer 2.8
Solara 2
Miranda 3.7-4
Colmo 4.2-5.3
Baccara 3.3-3.6
Allround 4.2
Radley 10.5 - 11.1
Baroness 9.4-10.6
Chantal 7.6-9.0
Heron 8.6-10.3 Alaska sweet 7.1
Maro 6.2-10.6 667 7.3
Progreta 7.0-9.6

Pisumabyssinicum L 808 12.8-13.2

JI 227 13.5-14.5

Winter type Frimas 8.2 - 12 Frogel 5.7-9.4

Frisson 9.0-15
Vendevil 6.7-8.6
Midiver 6.6-7.1
Printiver 8.5
Frilene 7.9-9.7
Amac 6.8-8.2
Rafale 8.1-9.8
Frijaune 8.3-12.7
Mistral 11.0-11.4
Brevent 3.9-5.3
Triolo 2.8-3.4
Booster 2.8-3.7

have been identified in this study including: Kelve- With 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

don wonder and Gullivert. Thus we can list physio- 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 distinguishable by differential hosts. This resistance seems stable.

Table 5
Physiological races of Ascochytapisi and differential hosts (Cousin et al., 1985)
Physiological races (Dr Hubbeling) D -- -- -- C B E
Name of strain No. 1 Several strains No. 4 No. 14 Tezier -- --
(12)
Gullivert R R R R S R R
Rondo R R S VLS R R S
Finale R R S LS R
Kelvedon wonder R S S S S R R
Dark-skinned perfection S S S S S R S
Arabal, Cobri, Starcovert, Supcovert, Vitalis S S S S S S S

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

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

In contrast, breeding for resistance to My- is controlled by a single recessive gene. Cousin
cosphaerella pinodes has been unsuccessful. (1965a) studied the reaction of about 400 pea culti-
Ali et al. (1978), in Australia, mention resistance vars to E. polygoni and found that some lines of
of some lines to strains o f M. pinodes. However, Mexican and Peruvian peas were nearly immune and
these lines are infected by strains isolated in France Stratagem lightly symptoms. This resistance is also
(Cousin et al., 1992c). In France, several thousand controlled by a single recessive gene. It seems that
lines were tested for their susceptibility to this dis- the difference in behavior of Mexican lines and
ease. Only a few lines show light symptoms. Stratagem is related to different alleles at the same
locus. In France, this resistance has been stable since
3.1.2. Downy mildew 1965.
D o w n y mildew caused by Peronospora viciae.
appears when the weather is cold (below 14°C) and 3.1.4. Fusarium wilt
wet, and may be severe in U.K., Netherlands, Swe- Pea wilt is caused by several races of Fusarium
den, France, New Zealand and Northwestern USA. oxysporum f.sp. pisi, occur mainly in North Amer-
White and Raphael (1944) reported that a few pea ica, the Netherlands and Belgium.
cultivars were resistant under the growing conditions This fungus has a large genetic variability, with
of Tasmania. Dixon (1981) indicated that some vari- race 1 the oldest, the most widely distributed and the
eties show light symptoms. Cousin (1974) shows that most aggressive. Resistance to this race is controlled
some varieties (Cobri, Starnain, Starcovert, Clause by a single dominant gene. Then Fusarium oxyspo-
50) are resistant and that this resistance is controlled rum f.sp. pisi race 2 appeared and caused near wilt
by a single recessive gene. This resistance seems to (Snyder and Walker, 1935). Another source of resis-
belong to the hypersensitivity type. tance controlled by a single dominant gene discov-
ered by Hare et al. (1949) again allowed breeding
3.1.3. Powdery mildew resistance to near wilt then released the Delwiche
Powdery mildew, caused by Erysiphe polygoni is C o m m a n d o variety resistant to wilt and near wilt.
significant wherever peas are grown. It is especially Hagedorn (1953) obtained the canning pea cultivar
troublesome in environments with warm dry days New Era. Race 3 (Schreuder, 1951), and race 4
and cool nights. (Bolton et al., 1966) appeared. A new variety, New
Resistance to powdery mildew was reported by Wales, was selected which is resistant to the three
Harland (1948) in Peruvian peas, and by Pierce races 1 - 2 and 4. N o w most pea cultivars are resis-
(1948) in a selection from Stratagem. This resistance tant 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).
Race 1 Race 2 Race 3 Race 4 Race 5 Race 6
Lindford Snyder and Walter Schreuder Buxton Bolton Haglund
1928 1935 1951 1955 1966 1970
Onward S s s s S S
Wisconsin perfection R s s s S O
Dark skin perfection R s O O O O
Delwiche commando R R s s O O
New era R R O s S S
New Wales R R O O R S
Lines (Kraft, Haglund) R R O R R R

R: resistant.
S: susceptible to wilt.
s: susceptible to near wilt.
O: no information.
 R. Cousin~Field Crops Research 53 (1997) 111-130 123

minor importance. However, the disease remains an veloped leaflets, then mosaic with translucent spots.
important problem in areas where pea is not grown Finally, stem, foliage and pods are distorted.
in sufficiently long crop rotations. This is the case in Schroeder and Barton (1958) obtained tolerance
north-western Washington (USA) where pea crops but not immunity to PEMV by selection of G21 and
sometimes are grown every two years in the same G168 from PI 140295. This resistance, controlled by
field. In these conditions, races 5 and 6 appeared a single dominant gene, has not been commonly used
(Haglund and Kraft, 1970) which oblige plant breed- by plant breeders, since its use might result in the
ers to undertake a large program of selection against selection of more aggressive strains.
this disease. Kraft and Haglund (1978) have devel-
oped lines resistant to races 5 and 6 (Table 6). 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)
3.1.5. Pea mosaic
in Europe and the USA. The symptoms are severe
Pea mosaic is caused by Bean virus 2 (BV2),
plant stunting, chlorosis of the upper foliage and leaf
Bean yellow mosaic virus (BYMV), or Pea common
roll.
mosaic virus (PCMV). This disease is of minor
Hubbeling (1956) found that several cultivars were
importance. Symptoms vary according to the strains.
resistant and Drijfhout (1968) reported that resis-
Generally, Pea common mosaic virus strains show a
tance was controlled by a single recessive gene. This
typical mosaic with clear and dark green areas with-
resistance is stable.
out deformation of the leaves. With Bean yellow
mosaic virus strains, the mosaic is more diffuse.
3.1.8. Pea seed-borne mosaic
Some strains cause vein necrosis and wilt. This
A seed-borne mosaic virus disease of pea was
disease is aphid-borne. Legumes such as clover and
observed in the USA for the first time in 1968. Slight
alfafa are reservoirs. Winter pea varieties which are
mosaic and leaf curling are the characteristic symp-
less visited by aphids than spring pea varieties are
toms. Severe reduction in yield has been observed in
not infected.
the field in USA (Kraft and Hampton, 1980). This
Hagedorn (1951) reported that several varieties of
viral disease is the most widely spread and the most
the Perfection type were resistant to BYMV, Yen
important in the world, because it is transmitted by
and Fry (1956) and Johnson and Hagedorn (1958)
seed. Stevenson and Hagedorn (1971) discovered
showed that the resistance to BYMV in pea is con-
resistance in P.I. 193586 and 193835. Hagedorn and
trolled by a single recessive gene. Cousin (1965b)
Gritton (1973) reported that resistance to PSbMV is
reported that the resistance to PCMV in pea is also
controlled by a single recessive gene.
controlled by a single recessive gene. Barton et al.
At Versailles, the resistance to PSbMV seems to
(1964) demonstrated that resistances to BV2 and
be stable, but other strains have been already de-
PCMV are conditioned by the same gene. Cross-pro-
tected and other sources of resistance found. The
tection tests between PCMV and BYMV strains
sbm 2 and sbm 3 genes confer resistance to lentil
show a cross protection which indicates that these
strain PSbMV-L and sbm 4 to PSbMV-P4. The sbm 1,
two strains belong to the same virus. Many varieties
sbm 3 and sbm 4 genes belong to a cluster located on
possess this resistance which is stable. Since 1951,
chromosome VI while sbm 2 is linked to the gene mo
no strain has been identified that could break down
on chromosome II.
this resistance.
The chromosome-6 cluster includes the sbm-1,
sbm-3 and sbm-4 genes as well as the cyv-2 gene for
3.1.6. Pea enation mosaic resistance to clover yellow vein virus (CYVV) (Pro-
Pea Enation mosaic disease is caused by Pea vvidenti and Muehlbauer, 1990). The chromosome-2
enation mosaic virus (PEMV) also named virus 1. cluster includes sbm-2, cyv for resistance to CYVV,
This virus produces characteristic blister-like ridges and mo for resistance to been yellow mosaic virus,
called 'enations' on the underside of leaves. The first as well as genes conferring resistance to others po-
symptom is vein cleating appearing on recently de- tyviruses (Provvidenti, 1990). The resistance gene-
124 R. Cousin/Field Crops Research 53 (1997) 111-130

cluster containing sbm-1 has been assigned to chro- Table 7

mosome-6 as a result o f linkage studies using a Physiological races of Pseudomonas syringae and differential
hosts
number o f chromosome-6 morphological and al-
lozyme markers including wlo (Gritton and Hage- Race1 Race2 Race3 Race4 Race5 Race6
dorn, 1975) and Prx-3 ( W e e d e n et al., 1991). Lincoln R R R R R S
Recently, the nucleotide sequence and deduced Progreta R R R S R S
Abador R R S R R S
amino acid sequence of pathotype P-4 were determi- Partridge R S R R R S
nated and compared to the corresponding sequences Belinda R S R S S S
of pathotype P-1 (Johansen et al., 1996). Early onward S R S S R S
P.abyssinicum R R R R R R
3.1.9. Pea early browning virus
This disease is known in the north o f Europe:
England and the Netherlands. tively by single recessive genes. F r o m the Lincoln ×
Veins of stipules and leaflets become necrotic and Belinda cross, the resistance to race 5 was found to
localized wilting appears. Symptoms may be re- be controlled by a single recessive gene. The domi-
stricted to a few leaves or a portion o f the leaves or nant gene which gives resistance to race 2 also
stipules. Pods show a purple-brown necrotic pattern. confers resistance to race 5. The recessive gene
This virus might be transmitted by the nematodes which gives resistance to race 3, also confers resis-
Trichodorus teres (Van Hoof, 1962). tance to race 1. Finally, the resistance to race 6 in
Pisum abyssinicum is also controlled by another
3.1.10. Bacterial blight recessive gene (Cousin et al., 1995).
Bacterial blight is caused by Pseudomonas sy-
ringae pv. pisi. This disease appears in particular on 3.1.11. Molecular markers
winter peas. But it can also occur on spring peas. P. In order to facilitate breeding for disease resis-
syringae pv. pisi was isolated from 20% of the field tance, research for molecular markers linked to resis-
pea crops sampled in the W i m m e r a region of Victo- tant genes has been carried out (Dirlewanger et al.,
ria, Australia (Hollaway and Bretag, 1995). In U.K. 1994). R L F P markers p252, p254, p248, p227, p105,
the incidence of infection, across all categories o f p236 and R A P D markers H19, Y14, Y I 5 are found
seed tested has highly increased over the last eight linked to resistance genes mo, Fw, er. Some QTL
years from 8.2% infected to 36.5%. Race 2 o f the
pathogen was most frequently isolated from infected
I II IV VI
seed samples and often associated with race 6 (Reeves
.H19 - - p236
et al., 1996). 6.2

N o w seven physiological races are known. In 14.4 15.9 9.4

• . Y14
9.B

er
1993, a source o f resistance to race 6 was found by
I I p252 • ' FW
R. Cousin and J. Schmit in France and J. Taylor in 6.0
• ~p254
England in some lines o f Pisum abyssinicum (Cousin 4 . 0 . p248 30.0

et al., 1995; Schmit et al., 1993). Thus, we now have

13.7
all the differential hosts with which to identify
I QTL concerning
physiological races (Table 7). Ascochytablight Y15
!
sbm-1
sbm-3
The segregation analyses of F 3 lines from crosses sbm-4
between differential hosts have enabled the genetic 12"51 3227
study of specific resistances. The resistances to race
1 and race 2 studied in the Lincoln × Early Onward 105
and Lincoln × Partridge crosses are controlled re-
Fig. 12. Partial genetic linkage map of pea constructed with
spectively by single dominant genes. Resistances to
MAPMAKER. Resistance genes and markers are on the right side
race 3 and race 4 studied in the Lincoln × A b a d o r of the chromosome and distances given in cM are on the left.
and Lincoln × Progreta crosses are controlled respec- (Didewanger et al., 1994).
 R. Cousin/Field Crops Research 53 (1997) 111-130 125

were also mapped for resistance to Ascochyta pisi 3.2. Environmental stress tolerance
race c (Fig. 12).
In the same way Timmerman et al. (1994) identi-
The improvement of yield stability in many grain
fied a RAPD marker (PD10650) tightly linked to
legume species and especially in dry pea is a major
powdery mildew resistant gene: er, and the RFLP
breeding objective. Cold and drought are the most
marker GS185 closely linked to sbm-1 (Timmerman
important environmental stresses.
et al., 1993).

3.2.1. Cold resistance

3.1.12. Transformation The performance of the many pea cultivars is
Transformation in legume is especially difficult. considerably affected by cold. Most lines and culti-
However, some transformants have been obtained by vars are very susceptible to cold, especially early
Schroeder et al. (1993) and more recently by Grant lines or lines with long internodes, large leaf area or
et al. (1995). However the application of this tech- wrinkled seeds. Only a few lines from wild Pisum
nique remains problematic. species or forage winter pea, probably originating

• Fodderpea parental8enotypes
D Winter pea parentalgenotypes
lOO

/
/ •••e•devil
r~/~
~ Champagne
Austrianwinter
• Springpea parentalgenotypes
/ ~D~ Frisson
7 ~BCam/~//~ wink°ssa

o ~ ivil
Colmo

i
0 5O 100
Variance (Vr)
2OO
Vendevilt2
:Champagne
150
FrissonD / / / Austrian winter

+ 100
>-
c /
50 /I Merlivil
Pilet 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.
126 R. Cousin/Field Crops Research 53 (1997) 111-130

Specific combining ability 2.0

with winter cullivars:
• Frisson

t
1.5
zx Vendevil .~

ttt
.N

• Winkossa
C 1.0
e,,¢
.0
E
El General combining 8
ability of spring
cultivars
(a 0.5

0.0
l
-0.5

I I I I I 1 I I I I I I I I I I I I .... I I
°
.~.~ E,~ _-~ ~ ~ ~-.~-~'~ ~ ~ ~
- g -~ ~- -=

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 dertaken. First, we looked for high combining ability
include Champagne and Haute-Loire from France, between spring and winter cultivars (Fig. 14). Then
Fenn and Melrose from the USA and Austrian winter cultivars which showed a high general combining
from Austria. ability were intercrossed, using a circular crossing
Winter hardiness in the P i s u m species is reported scheme in order to bring together the most cold
to be a quantitatively inherited trait (Auld et al., resistance genes (Fig. 15). Lastly, progenies were
1983; Cousin, 1983; Markarian and Andersen, 1966). selected under field conditions and under controlled
The study of the progeny of crosses between spring conditions (Cousin et al., 1993c).
peas and Champagne or Haute-Loire showed that it In order to assess cold resistance, a selection
is possible to transfer cold resistance from the fodder method under controlled conditions was developed
winter pea to vining or combining peas.
The analysis of diallel crosses showed that cold Mihan Anik

resistance is a quantitative character, with intermedi-

ate dominance. All lines are distributed along a swa°99'°°l
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 Winkossa
greater cold resistance than their parents were se-
lected. Frisson Hativer
The quantitative character for cold resistance hav- Fig. 15. Circular crossing scheme used to breed pea cultivars with
ing been demonstrated, recurrent selection was un- high levels of cold resistance.
 R. Cousin~Field Crops Research 53 (1997) 111-130 127

by Prieur and Cousin (1978). Before exposing plants mined. The use of the afila gene has contributed to a
to the required minimum temperature, we subjected decrease in leaf area and an increase in yield. Resis-
them to a progressive decrease in temperature over a tance to lodging remains to be improved. The num-
period of 2 - 3 weeks so that they became hardened. ber of fertile nodes must be reduced, perhaps by
After the plants had been subjected to below-zero introducing genes that determine plant growth.
temperatures, for varying periods, the temperature Assimilation and nitrogen fixation are well under-
was gradually increased. This method makes easier stood. However, factors limiting seed filling in some
the classification of different lines according to their varieties or those reducing the nitrogen remobiliza-
degree of cold resistance. tion from leaves to seeds when the biomass produc-
Several characters seem to be associated with tion is high, remain to be found.
winter hardiness. Pigmented hilums conditioned by a Cold and disease resistance have been greatly
dominant gene, Pl, on chromosome VI were strongly improved. However new improvements remain pos-
associated with winter hardiness Liesenfeld et al. sible as the selected winter pea cultivars are still less
(1986); Markarian and Andersen (1966). Pigmented resistant to cold than resistant wild pea germplasms.
seed coats and yellow cotyledons, conditioned by the Effective resistance to Ascochyta blight caused by
dominant genes A and I, respectively, on chromo- Mycosphaerella pinodes, root rot caused by
some 1, were associated with cold resistance. Murray Aphanomyces euteiches, or pea enation mosaic virus,
et al. (1988). Powdery mildew resistance conditioned remains elusive. In these cases classical breeding by
by the recessive gene er on chromosome V1 seems vertical gene management cannot be undertaken.
to be linked to the major susceptible gene (D.L. Finding polygenic resistance or transferring artificial
Auld, personal communication). The same linkage resistance genes should be investigated.
has been noted for greater amounts of trypsin in- Research concerning pea transformation needs to
hibitors in seeds, but, in many cases, these linkages be increased. This should, for example, allow the
have been broken. introduction into peas of resistances to insects, viruses
or herbicides against which there is no natural resis-
3.2.2. Drought tolerance tance.
Drought stop the nitrogen fixation and decreases Wide variability exists for seed constituents in
the biomass production (Cousin et al., 1993c). peas. Peas constitute an important source for feed
Biarnes Dumoulin et al. (1996) in a study of 10 and food manufacturers. The range of different uses
genotypes sown at two dates during two years at of peas could be increased. Breeding for varieties
three locations in France confirmed the existence of with very thick edible pod could be considered a
high variability for yield. The environmental effect good strategy for finding a new vegetable. Research
was preponderant and essentially due to differences for increasing amylose content in pea seeds may also
of soil water availability during the flowering period. be a strategy for obtaining the new biodegradable
The genotype × environment interaction is deter- plastic materials used by car manufacturers.
mined by the differential response of genotypes,
according to their earliness to flower and the dura-
tion of the seed set period, when grown under drought
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