ISSN 0003-6838, Applied Biochemistry and Microbiology, 2007, Vol. 43, No. 3, pp. 237–243. © Pleiades Publishing, Inc., 2007.
Original Russian Text © A.Yu. Borisov, T.N. Danilova, T.A. Koroleva, E.V. Kuznetsova, L. Madsen, M. Mofett, T. S. Naumkina, T.A. Nemankin, E.S. Ovchinnikova, Z.B. Pavlova,
N.E. Petrova, A.G. Pinaev, S. Radutoiu, S.M. Rozov, T.S. Rychagova, O.Yu. Shtark, I. I. Solovov, J. Stougaard, I.A. Tikhonovich, A.F. Topunovf, V.E. Tsyganov, A.G. Vasil’chikov,
V.A. Voroshilova, N.F. Weeden, A.I. Zhernakov, V.A. Zhukov, 2007, published in Prikladnaya Biokhimiya i Mikrobiologiya, 2007, Vol. 43, No. 3, pp. 265–271.
237
Garden pea is important not only as a valuable agri-
cultural plant, but also as a model for genetic and phys-
iological studies, including in the field of mutualistic
plant–microbial interactions. During evolution, pea
acquired the capacity for forming two types of mutual-
istic endosymbioses: (1) a nitrogen-fixing symbiosis
(NFS) with the root nodule bacterium Rhizobium legu-
minosarum bv. viciae and (2) arbuscular mycorrhiza
(AM) with fungi belonging to the phylum Glomerulo-
mycota [1]. This allows the plant to exist under the con-
ditions of decreased soil fertility, where the microsym-
biont providing the plant with nutrients gets in
exchange products of photosynthesis and an ecological
niche. The symbioses also prevent soil exhaustion and
maintain the biodiversity of plant communities [2–4].
Both NFS and AM are characterized by a high degree
of integration of the genetic systems of the partners and
largely controlled by the plant [5].
Identification of symbiotic pea genes controlling
NFS formation. Analysis of genetic variability of sym-
biotic properties of pea plants was pioneered by
Govorov [6] and Razumovskaya [7], who found that
certain genotypes of pea from Afghanistan (which
belongs to the Central-Asian center of origin of culti-
vated plants) are associated with failure of the plants to
form nodules with certain strains of root nodule bacte-
ria inhabiting European soils (other plants from the
region, differing in their genotype, did form the nod-
ules). Genetic analysis of local Afghan specimens, per-
formed by Lie [8], made it possible to identify the first
symbiotic pea genes (Sym). The wide use of chemical
and physical mutagens furthered the identification of
new symbiotic pea genes.
Programs completed in several laboratories all over
the world, in which a variety of methods of mutagenesis
and diverse specimens and strains of pea plants were
used (reviewed in [9], have thus far produced more than
250 mutants [10–29]. About one half of them were
included into a complementation analysis, which
resulted in identifying in excess of 40 symbiotic genes
(Table 1).
Intensive morphological analysis of the mutants iso-
lated demonstrated that certain stages of nodule devel-
opment were blocked [17, 20, 21, 23, 25, 26, 30–38].
Based on our results and data reported in the literature,
nodule morphogenesis may be separated into two
Regulatory Genes of Garden Pea (Pisum sativum L.) Controlling
the Development of Nitrogen-Fixing Nodules and Arbuscular
Mycorrhiza: A Review of Basic and Applied Aspects
A. Yu. Borisov
a
, T. N. Danilova
a
, T. A. Koroleva
a
, E. V. Kuznetsova
a
, L. Madsen
c
, M. Mofett
d
,
T. S. Naumkina
b
, T. A. Nemankin
a
, E. S. Ovchinnikova
a
, Z. B. Pavlova
a
, N. E. Petrova
f
,
A. G. Pinaev
a
, S. Radutoiu
c
, S. M. Rozov
e
, T. S. Rychagova
a
, O. Yu. Shtark
a
, I. I. Solovov
b
,
J. Stougaard
c
, I. A. Tikhonovich
a
, A. F. Topunov
f
, V. E. Tsyganov
a
, A. G. Vasil’chikov
b
,
V. A. Voroshilova
a
, N. F. Weeden
d
, A. I. Zhernakov
a
, and V. A. Zhukov
a
a
All-Russia Research Institute of Agricultural Microbiology, Russian Academy of Agricultural Sciences,
St. Petersburg, 196608 Russia; e-mail: Alexey_Borisov@arriam.spb.ru
b
All-Russia Research Institute of Grain Legumes and Groats Crops, Russian Academy of Agricultural Sciences,
Orel, 302502 Russia; e-mail: Naumkina1@yandex.ru
c
Aarhus University, Department of Molecular Biology, DK-8000, Aarhus C, Denmark; e-mail: stougaard@mb.au.dk
d
Montana State University, Bozeman, Montana, USA; e-mail: nweeden@montana.edu
e
Institute of Cytology and Genetics, Siberian Division of the Russian Academy of Sciences, Novosibirsk, 630090 Russia;
e-mail: rozov@bionet.nsc.ru
f
Bach Institute of Biochemistry, Russian Academy of Sciences, Moscow, 119071 Russia; e-mail: topunov@inbi.ras.ru
Received July 11, 2006
The review sums up the long experience of the authors and other researchers in studying the genetic system of
garden pea (Pisum sativum L.), which controls the development of nitrogen-fixing symbiosis and arbuscular
mycorrhiza. A justified phenotypic classification of pea mutants is presented. Progress in identifying and clon-
ing symbiotic genes is adequately reflected. The feasibility of using double inoculation as a means of increasing
the plant productivity is demonstrated, in which the potential of a tripartite symbiotic system (pea plants–root
nodule bacteria–arbuscular mycorrhiza) is mobilized.
DOI: 10.1134/S0003683807030027