directly or indirectly through the BZR1 family)
leads to higher BIN2 activity and derepression
of SPCH, promoting accumulation of SPCH in
active meristemoids (Fig. 4F). Overall, this feedback mechanism by SPCH would serve to reinforce
differences between SPCH-expressing meristemoids
and nonexpressing neighbors, which may be important for local patterning and coordinating the
lineage with overall BR-mediated growth controls.
Here, we revealed the broad influence of SPCH
in stomatal lineage specification through MOBE-ChIP. This technique, which is based on a simple
scale increase, could be widely applicable in other
tissues or organisms to obtain high-quality binding
information about cell-type–specific regulators.
The large number of SPCH-binding regions reported here is reminiscent of the behavior of the
bHLH transcription factor MyoD, a master regulator of mammalian myogenesis, which associates with more than 30,000 regions in the human
genome and is responsible for resetting global
transcriptional and epigenetic states during development (29). Additional experiments are needed
to establish definitively how often and by what
mechanisms SPCH binding alters gene expression. However, our data that hundreds of genes,
including those mediating abiotic and hormone
responses, are directly regulated by SPCH supports previous functional studies (20, 22) that
place SPCH in a critical position to integrate physiological and environmental information into a
developmental program that optimizes leaf properties (stomatal density and size) for prevailing
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We thank Z.-Y. Wang (Carnegie) for the antibody to YFP and
the bin2-1 allele; Y. Yin (Iowa State University) for the BES1pro:
bes1-D-GFP construct; J. Chory (SALK) for the bes1 RNAi line;
and members of our laboratory for critical comments. Funding
for this work was provided by National Institutes of Health (NIH)
1R01GM086632. O.S.L. was a Croucher Fellow, K.A.D. was
supported by Cellular and Molecular Biology Training Program
NIH5T32GM007276 and by a National Science Foundation
graduate research fellowship, and J.A. was supported by the DAAD.
D.C.B. is a Gordon and Betty Moore Foundation Investigator of the
Howard Hughes Medical Institute. The ChIP-seq and RNA-seq data
in this study can be found in National Center for Biotechnology
Information’s Gene Expression Omnibus repository ( www.ncbi.nlm.
nih.gov/geo) as GSE57954. The supplementary materials contain
Materials and Methods
Figs. S1 to S15
Tables S1 to S8
3 June 2014; accepted 25 August 2014
Published online 4 September 2014;
Early Levallois technology and the
Lower to Middle Paleolithic
transition in the Southern Caucasus
D. S. Adler,1 K. N. Wilkinson,2 S. Blockley,3 D. F. Mark,4 R. Pinhasi,5
B. A. Schmidt-Magee,1 S. Nahapetyan,6 C. Mallol,7 F. Berna,8 P. J. Glauberman,1
Y. Raczynski-Henk,9 N. Wales,1,10 E. Frahm,11 O. Jöris,12 A. MacLeod,3 V. C. Smith,13
V. L. Cullen,13 B. Gasparian14
The Lower to Middle Paleolithic transition (~400,000 to 200,000 years ago) is marked
by technical, behavioral, and anatomical changes among hominin populations throughout
Africa and Eurasia. The replacement of bifacial stone tools, such as handaxes, by tools
made on flakes detached from Levallois cores documents the most important conceptual
shift in stone tool production strategies since the advent of bifacial technology more
than one million years earlier and has been argued to result from the expansion of
archaic Homo sapiens out of Africa. Our data from Nor Geghi 1, Armenia, record the
earliest synchronic use of bifacial and Levallois technology outside Africa and are
consistent with the hypothesis that this transition occurred independently within
geographically dispersed, technologically precocious hominin populations with a
shared technological ancestry.
The Late Middle Pleistocene [LMP, oxygen isotope stage (OIS) 12/11e to OIS 6/5e, ~425 to 130 thousand years ago (ka)] witnessed the evolution of Homo sapiens in Africa and Neandertals in western Eurasia (1, 2). In
Africa, the Early Stone Age (ESA)–Middle Stone
Age (MSA) transition is characterized by the slow
replacement of bifaces by flakes, points, and
blades produced through various hierarchical
core reduction strategies, among which Levallois
concepts are the most notable (3–6). In Western
Europe, lithic assemblages from Late Acheulian
contexts highlight the asynchronous, geographi-
cally discontiguous evolution from bifacial to
Levallois technology and the gradual transition
from the Lower Paleolithic (LP) to the Middle
Paleolithic (MP) ~300 to 200 ka (7–9). Levantine
sites assigned to the Acheulo-Yabrudian (AY, ~400
to 200 ka) document non-Levallois methods for
the manufacture of blades, broad flakes, and thick
scrapers with scalar retouch (Quina) and the grad-
ual disappearance of bifaces (10, 11). The techno-
logical variability apparent in these regions reflects
the complex hominin behavioral mosaic in place
before the MSA and the MP (12) (Fig. 1). Within
the Southern Caucasus, a region situated between
Africa and Europe, this critical period of techno-
logical and behavioral evolution remains un-
charted and undated (13).
In bifacial technology (Mode 2), a mass of stone
is shaped through the serial removal of interrelated flakes (façonnage) until the remaining
volume takes on a desired form, such as a handaxe.
This method of stone tool production originated in
Africa ~1.75 million years ago and spread to Eurasia
with the initial Acheulian dispersal <900 ka. In
contrast, Levallois technology (Mode 3), a specific hierarchical core reduction strategy, entails
the multistage shaping (façonnage) of a mass of
stone (core) in preparation to detach a flake of
predetermined size and shape from a single preferred surface (débitage) (14, 15). Flakes resulting
from biface production were generally treated as
waste, whereas particular flakes detached from a