J. PlantPbysiol. Vol. 137. pp. 389-396 (1991)
Mature Nodules and Root Tips Control Nodulation in Soybean
GUSTAVO CAETANO-ANOLLES\ ELLEN T. PAPAROZZI
2
, and PETER M. GRESSHOFF
Plant Molecular Genetics (OHLD), Institute of Agriculture and Center for Legume Research, The University of
Tennessee, Knoxville, Tennessee 37901-1071
Received May 25, 1990 . Accepted August IS, 1990
Summary
Nodule formation in soybean (Glycine max (L.) Merr.) is suppressed in younger regions of the root
system as a feedback response to development of first nodules. Removal of functional nodules caused al-
ready initiated to develop into mature nodules, in the same regions of the roots where the in-
itial nodules were formed. This was true for soybean cv. Bragg and the supernodulating mutant derivative
nts382. In experiments where the tips of the lateral roots of Bragg were removed before or at inoculation,
nodulation on the primary root was considerably increased. In contrast, removal of the lateral root tips
from nts382 had no effect. Our results suggest that nodulation in soybean is preferentially controlled by
the arrest rather than the abortion of early subepidermal cell division during nodule development, and
that both mature nodules and root apical meristems elicit feedback regulation of nodule formation.
Key words: Bradyrhizobium japonicum; feedback regulation; nodulation; Glycine max; symbiosis; root me-
ristems.
Abbreviations: EH = smallest emergent root hair; RT = root tip; RDU = relative distance unit.
Introduction
Soybean (Glycine max (L.) Merr.) plants are able to form
nitrogen-fixing root nodules in close association with bac-
teria of the genus Bradyrhizobium. The establishment and
function of the nodule results from the coordinate exchange
of information between the symbionts in the way of signal
molecules, which initially results on root hair curling and in-
fection thread formation (Long, 1989). Prior to these host re-
sponses, cortical cells beyond the site of the incipient infec-
tion are induced to redifferentiate and divide to form a
nodule primordium (Turgeon and Bauer, 1982; 1985). These
cell division foci occur even in the absence of local root hair
curling and infection (Calvert et aI., 1984; Mathews et aI.,
1989). Several tranposon-induced Rhizobium and Bradyrhizo-
bium mutants as well as Agrobacterium strains harboring
cloned nodulation genes were found to induce nodules with-
out infection threads and intracellular bacteria (Truchet et
I Corresponding author.
2 Present address: Department of Horticulture, University of
Nebraska, Lincoln, Nebraska 68583-0724.
© 1991 by Gustav Fischer Verlag, Stuttgm
al., 1984; Hirsch et aI., 1984; Finan et aI., 1985; Stanley et aI.,
1986). Based on these and other observations, infection and
cell division were considered to be uncoupled events.
The host plant controls the timing, frequency and success
of infection. In soybean, the region most susceptible to infec-
tion and nodulation by rhizobia coincides with the zone of
elongation of the root (Bhuvaneswari et aI., 1980; 1981),
where epidermal cells with immature or as yet unformed
root hairs are the usual sites of bacterial penetration (Tur-
geon and Bauer, 1982). This susceptible region moves along
with root development defining a developmental time
window in which root cells are transiently susceptible to in-
fection. However, the roots are unable to support nodula-
tion once first infections are established (Pierce and Bauer,
1983). Many more cell division foci are formed than ever be-
come infected or result in an emergent nodule (Calvert et aI.,
1984; Mathews et aI., 1989). The mechanism that controls
the progress of infection has been termed autoregulation or
feedback suppression of nodule formation and is elicited
systemically (Kosslak and Bohlool, 1984; Olsson et aI., 1989)
when cortical cell division foci are induced in the roots
(Caetano-Anolles and Gresshoff, 1990). The systemic nature