INSIGHTS | PERSPECTIVES974 4 MARCH 2022 • VOL 375 ISSUE 6584GRAPHIC: KELLIE HOLOSKI/SCIENCEscience.org SCIENCEBy Lidor Shaar-Moshe1,2and
Siobhan M. Brady1,2P
lants continuously elaborate their
form through the production of new
organs, including different types of
roots. A primary root emerges from
a seed, and lateral roots develop post-
embryonically from the primary root
axis. In addition, plants can generate a vari-
ety of shoot-borne roots. These are called ad-
ventitious roots ( 1 ) in dicotyledonous plants,
such as tomato, or crown and brace roots
( 2 ) in monocotyledonous cereal crops, such
as maize or sorghum. But the developmen-
tal mechanisms associated with shoot-borne
root initiation as well as the conservation of
this program with lateral and wound-induced
roots are largely unknown. On page 993 of
this issue, Omary et al. ( 3 ) report a conserved
developmental pathway for shoot-borne
roots across flowering plants
and a conserved “superlocus”
that regulates the initiation of
specialized root types.
Lateral roots derive from
pericycle cells that flank xylem
cells (which transport water)
within the root. By contrast,
Omary et al. demonstrate that
in tomato (Solanum lycoper-
sicum), shoot-borne roots de-
rive from cells located around
the phloem (which transports
nutrients), called the phloem
parenchyma. Hormone (auxin
and cytokinin) signaling con-
tributes to the formation of a
properly patterned root pri-
mordia, which includes the
formation of a stem cell niche
and asymmetric divisions of
stem cells to produce root cell
types. To determine how fields
of hormone-responsive cells
change through shoot-borne
root primordia development,
Omary et al. used hormone-
response markers. Similarity
in the cellular response fieldsbetween lateral root and shoot-borne root
primordia would demonstrate conserved
mechanisms of root primordia. As the shoot-
borne root primordia undergoes cell pat-
terning, cells within the primordia respond
to auxin or cytokinin or both. In tomato lat-
eral root initiation, there is no overlap in the
cytokinin- and auxin-responsive domains,
similar to Arabidopsis thaliana ( 4 ). Thus, the
cells and hormonal signaling that give rise to
shoot-borne and lateral root primordia differ,
suggesting that these two developmental pro-
grams are different.
Omary et al. carried out single-cell tran-
scriptome profiling of shoot-borne root pri-
mordia over developmental time, which re-
vealed a group of cells with an ephemeral cell
identity. These cells share a transcriptional
enrichment for root stem cell regulators, and
a developmental trajectory analysis identi-
fied this cell group as a branch point for dif-ferent identities. Thus, Omary et al. called
them “transition stem cells”; they are the
intermediary stage between phloem paren-
chyma cells and shoot-borne root primordia
initial cells. This transitional state served as
a platform to identify potential regulators,
including a transcription factor belonging
to the LATERAL ORGAN BOUNDARIES
DOMAIN (LBD) family ( 5 ) that the authors
named SHOOTBORNE-ROOTLESS (SBRL).
They demonstrated that SBRL is necessary
for shoot-borne root, but not lateral root, ini-
tiation in tomato. The function of SBRL or-
thologs was conserved in other dicotyledon-
ous species, potato, and A. thaliana and likely
conserved in sweet potato, white bean, and
the monocot sorghum. Monocots and dicots
had a most recent common ancestor ~150
million years ago. The identical function of
this gene across such a long evolutionary
time demonstrates substantial conservation.
The analysis by Omary et al. of tomato
SBRL and its orthologs indicated that
shoot-borne and lateral root developmen-
tal programs are quite different. However,
a phylogeny of LBD transcription factors
demonstrated that SBRL belongs to subclass
IIIB of LBD transcription factors. When as-
sembling this phylogeny, the authors noted
that a subclass IIIB gene was nearly always
located next to a closely related
subclass IIIA gene, which they
called an LBD superlocus, with
conserved regulatory elements.
Subclass IIIA genes are associ-
ated with lateral root initiation
in maize and A. thaliana ( 6 ).
Do subclass IIIA genes also
regulate a transition stage in
lateral root initiation? Omary
et al. found that expression of
a large proportion of a gene
set that defines the transition
state was induced in analogous
stages of lateral root initiation.
Mutation of the tomato sub-
class IIIA gene BROTHER OF
SBRL (BSBRL) and its paralog
BSBRL2 reduced lateral root
initiation, with no change to
shoot-borne roots. Mutation of
the A. thaliana subclass IIIA
gene resulted in an equivalent
phenotype. The local duplica-
tion that gives rise to these
neighboring subclass IIIA and
IIIB genes therefore allowed
the evolution of two indepen-
dent root-initiation programs
from distinct parts of the plant
body across diverse flowering
plant species.
A third wound-induced root
type is critical to agriculturePLANT BIOLOGYForming roots from shoot
Uncovering the genes responsible for different types of
roots will transform aspects of plant agriculture
(^1) Department of Plant Biology, University
of California, Davis, Davis, CA, USA.
(^2) Genome Center, University of California,
Davis, Davis, CA, USA. Email: lshaar@
ucdavis.edu; [email protected]
Shoot-borne root
Wound-induced root
Lateral root
IIIA IIIB
IIIA IIIB
IIIA IIIB
Xylem
Pericycle
Cambium
Endodermis or
starch sheath
Phloem
Formation of specialized root types
The LATERAL ORGAN BOUNDARIES DOMAIN (LBD) superlocus regulates root
development by inducing a transition state. Lateral root initiation depends on
expression of LBD IIIA genes in the xylem pole–pericycle. Shoot-borne root initiation
depends on expression of LBD IIIB genes in phloem-associated cells. Both LBD IIIA and
IIIB genes are required for initiation of wound-induced roots.