INSIGHTS | PERSPECTIVESsciencemag.org SCIENCEGRAPHIC: V. ALTOUNIAN/SCIENCEBy Patricia Baldrich^1 and
Blake C. Meyers1,2S
tudied for more than 130 years ( 1 ),
the intimate and unusual relation-
ship established between legumes
and nitrogen-fixing bacteria (Rhizo-
bia) allows plants to use atmospheric
nitrogen in exchange for their pho-
tosynthetic-derived carbohydrates. The
production of root nodules in which the
symbiotic interaction takes place requires
complex developmental regu-
lation by the plant. Nodules
are relatively distinct organs
among plant species, essen-
tially representing a controlled
microbial invasion of the root.
Somewhat like the human gut,
the plant provides an environ-
ment in which specific mi-
crobes can thrive—but unlike
the gut, nodule microbial com-
position is limited to a small
number of species. The genetic
control of nodulation develop-
ment is complex, with recent
work showing a dependency on
small RNAs (sRNAs) trafficked
from shoot to root ( 2 ). On page
919 of this issue, Ren et al. ( 3 )
identify bacteria-derived trans-
fer RNA (tRNA)–derived frag-
ments (tRFs) as modulators of
the process of nodulation.
In plants, sRNAs are classified
into at least three pathways: mi-
croRNAs, heterochromatic short-
interfering RNAs (hc-siRNAs),
and phased secondary siRNAs
(phasiRNAs). All three of these
pathways require the enzyme Dicer, which
processes longer RNAs into smaller RNAs.
However, since the earliest days of large-
scale RNA sequencing studies, a large
class of structural RNA fragments have
been identified but largely ignored. These
sequences, mostly originating from ribo-
somal RNAs and tRNAs, were considered
degradation products, unavoidably cap-
tured during RNA sequencing and of little
functional importance.
tRNAs are one of the most conserved and
abundant RNA species in cells; they func-
tion to decode messenger RNA (mRNA)
into proteins in ribosomes. tRNAs have adistinctive cloverlike structure, containing
three hairpin loops, with a specific amino
acid attached to the end that is used to
translate codons in the mRNA to an amino
acid transferred to the end of a growing
protein. During the tRNA biogenesis pro-
cess, or under specific conditions, cleavage
yields tRFs. These ~17- to 22-nucleotide
(nt) fragments have few known functions,
one of which is a role in genome protection
against transposable elements (TEs) ( 4 , 5 ).
TEs are widespread repetitive genome se-quences derived from viruses that have the
ability to mobilize. Their mobilization in
the “host” genome is typically suppressed
because the potential disruption of host
genome sequences (mutations or genome
rearrangements) might be detrimental for
fitness. The association of tRFs with the
ARGONAUTE (AGO) proteins that medi-
ate sRNA-target interactions has also been
described ( 6 ), as well as their Dicer depen-
dency ( 5 ), suggesting that tRFs function in
posttranscriptional control.
From sRNA sequencing data, Ren et al.
identified tRFs from the rhizobium Brady-
rhizobium japonicum, which are enrichedin planta and predicted to target 52 genes
in the soybean (Glycine max) genome.
Three of these genes—GmRHD3, GmHAM4,
and GmLRX5, which are orthologs of
Arabidopsis thaliana genes ROOT HAIR
DEFECTIVE 3 (RHD3), HAIRY MERISTEM
4 (HAM4), and LEUCINE-RICH REPEAT
EXTENSIN-LIKE 5 (LRX5), respectively—
are directly involved in development,
including that of root hairs. This is partic-
ularly important because nodulation starts
when the tip of a hair root curls around a
rhyzobial cell, creating a small
tube, the infection thread, that
will provide a path for the bac-
teria to reach the root epider-
mal cells. Ren et al. found that
the 21-nt tRFs produced by the
bacteria are loaded into the
soybean AGO1 protein, subse-
quently interacting with target
genes in a sequence homology–
dependent manner (see the fig-
ure). A series of experiments
demonstrated that these genes
are critical for the early stages
of the establishment of the
root nodulation process, and in
planta suppression of the tRFs
supports a role for them in pro-
moting the infection process.
To determine whether this
regulatory process is conserved
across evolutionarily related
nodulating legumes, Ren et al.
examined the compatible sym-
biotic interaction established
between the common bean and
its symbiotic partner, Rhizo-
bium etli. The authors found
that a different set of tRFs
target a different set of genes in this host
plant. These results suggest that the use of
bacterial tRFs to target host genes might
be conserved, whereas the tRFs and their
target genes may vary across species. These
findings, combined with previous studies
on plant sRNAs involved in the nodulation
process ( 2 ), highlight the complexity of the
regulatory network that occurs during the
establishment of nodulation.PLANT BIOLOGYBacteria send messages to colonize plant roots
Bacteria-derived RNA fragments target host plant genes to promote root colonization
(^1) Donald Danforth Plant Science Center, Saint Louis, MO 63132,
USA.^2 Division of Plant Sciences, University of Missouri–
Columbia, Columbia, MO 65211, USA. Email: pbaldrich@
danforthcenter.org; [email protected]
1 tRFs are produced from
the rhizobial tRNAs.
2 tRFs are transferred to
the plant cell via an as-
yet-unknown process.
3 tRFs are loaded in the
plant AGO1 protein to
facilitate RNA-RNA
interactions.
4 Rhizobial tRFs target
host genes, promoting
rhizobial infection.
Developmental transition
Root
Nodule
Rhizobium
Plant cell Bacterial cell
?
?
AGO
tRFs tRNA
Transfer of RNA fragments to plant cells
Transfer RNA (tRNA)–derived fragments (tRFs) are produced
from bacterial tRNAs and then transferred to the host plant cells,
where they bind Argonaute (AGO) proteins and silence host
genes to promote root nodule formation.
868 30 AUGUST 2019 • VOL 365 ISSUE 6456
Published by AAAS