PlantMolecular Biology 31:713-719, 1996.
@ 1996 Kluwer Academic"Publishers. Printed in Belgium.
713
Stringently and developmentally regulated levels of a cytoplasmic
double-stranded RNA and its high-efficiency transmission via egg and pollen
in rice
H. Moriyama, K. Kanaya 1, J.Z. Wang 2, T. Nitta* and T. Fukuhara
Laborato~ of Molecular Cell Biology, Faculty of Agriculture, To~'o University of Agriculture and Technology;
Fuchu, Tokyo 183, Japan (*author for correspondence); J Present address: Laborato©' of Glico Molecular
Biology, Frontier Research Program, The Institute of Physical and Chemical Research, Wako, Saitama 351-01,
Japan; 20n leave from Institute of Genetics, Academia Sinica, Bei/ing, PCR
Received24 October 1995;acceptedin revisedform8 April 1996
Key words: biparental transmission, copy number, cultured cell, cytoplasmic inheritance, double-stranded RNA,
Orvza sativa
Abstract
A very restricted amount of high-molecular-weight double-stranded RNA (dsRNA) has been tbund in healthy
japonica rice plants. We discriminated dsRNA-carrying rice plants from noncarriers. The endogenous dsRNA was
localized in the cytoplasm (about 100 copies per cell) and was transmissible to progeny plants by mating. In crosses
between carriers and noncarriers, the RNA was transmitted efficiently to F1 plants via both egg and pollen. The
rice dsRNA was maintained at an almost constant level by host plant cells from generation to generation. The
high-efficiency transmission of the endogenous dsRNA to progeny plants appears to depend on the autonomously
controlled replication of the dsRNA localized in cytoplasmic vesicles. However, an increase in copy number
(about 10-fold) of the dsRNA was observed during the suspension culture of host cells. The number of copies of
dsRNA returned to the original low value in regenerated plants, suggesting that the copy number is stringently and
developmentally regulated in rice cells.
Introduction
Endogenous double-stranded RNAs (dsRNAs) are dis-
tributed extensively in the plant kingdom, from algae
to higher plants [2, 5, 6, 10, 15]. Host plants with these
plasmid-like dsRNAs are apparently asymptomatic.
Although horizontal transmission of the dsRNAs from
plant to plant has not been proven, the dsRNAs are
known to be transmitted to progeny cells during cell
division [2].
Thus, the known endogenous dsRNAs are transmit-
ted vertically from generation to generation via seeds
[1]. The uniparental, namely, maternal, inheritance
of plant dsRNAs via seeds could be simply anticip-
ated when the dsRNAs are localized in the cytoplasm
[2]. However, the transmittance efficiency of the cyto-
plasmic dsRNAs during fertilization is distinct from
the efficiency of the cell organelles. Some of low-
molecular-weight dsRNAs, encapsidated by proteins to
form isometric particles, known as cryptoviruses, are
transmitted biparentally to progeny plants; the trans-
mission is generally found to be about 50% efficient
when noncarrier plants are pollinated by carriers [1].
Double-stranded RNAs that do not appear to be associ-
ated with distinct virus-like particles in the cytoplasm
are also transmitted biparentally in Phaseolus [14],
alfalfa [7], Brassica [16] and barley [24]. Thus, details
of the inheritance of the cytoplasmic dsRNAs should
be examined extensively in a variety of plants with
special reference of copy number and the subcellular
localization of the dsRNAs in host cells.
A high-molecular-weight dsRNA occurs in every
tissue and at every developmental stage in japonica rice
[8, 22, 23]. The rice of dsRNA of 13 952 nucleotides
(nt) in length has one, extremely long, open reading
frame (ORF) of 13 716 nt that appears to encode a large