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ACKNOWLEDGMENTS
We thank A. Treiman, C. Boschi, and three anonymous reviewers
for helpful comments during the preparation of this manuscript.
We also thank the Meteorite Working Group, now the Antarctic
Meteorite Review Panel of the Astromaterials Allocation Review
Board, for carefully evaluating our sample requests and the
curatorial staff at NASA Johnson Space Center for allocation of the
ALH 84001 samples used in this study. The US Antarctic meteorite
samples were recovered by the Antarctic Search for Meteorites
(ANSMET) program, which has been funded by NSF and NASA and
characterized and curated by the Department of Mineral Sciences of
the Smithsonian Institution and the Astromaterials Acquisition and
Curation Office at NASA Johnson Space Center, respectively. A.St.,
L.G.B., L.J.H., and A.C.O. thank Diamond Light Source for beam time
(run MG2444) and acknowledge the input and help of B. Kaulich and
M. Kazemian.Funding:A.St. acknowledges NASA grant
17-NAI8_2-0020 (principal investigator K.R.) and M. Walter (EPL)
for travel funding. L.G.B., R.W., and A.St. acknowledge financial
support for the TEM work through the Helmholtz Recruiting Initiative
program awarded to L.G.B. F.M.M. acknowledges support from
NASA’s Planetary Science Research Program.Author
contributions:A.St. collected data, performed data analysis, led
the study, and led the writing of the paper. L.G.B., T.A., S.V., R.W.,
A.Sc., L.R.N., J.W., L.J.H., F.M.M., and A.C.O. performed data collection
and analysis. F.M.M., M.D.F., P.G.C., C.C., V.R., and K.R. discussed
the interpretation of results and contributed to the writing of the
paper.Competing interests:There are no competing interests to
report for any of the authors.Data and materials availability:
The main mass of ALH 84001 is stored at NASA Johnson Space
Center, which makes samples available for research via https://
curator.jsc.nasa.gov/antmet/requests.cfm?section=general. The
FIB films we used are archived at the Carnegie Institution of
Washington. See ( 12 ) for further details. Our microscopy,
spectroscopy, and NanoSIMS data are archived at Dryad ( 37 ).
SUPPLEMENTARY MATERIALS
science.org/doi/10.1126/science.abg7905
Materials and Methods
Supplementary Text
Figs. S1 to S7
Tables S1 and S2
References ( 38 – 60 )
2 February 2021; accepted 17 November 2021
10.1126/science.abg7905
PLANT SCIENCEAn RNA exosome subunit mediates cell-to-cell
trafficking of a homeobox mRNA via plasmodesmata
Munenori Kitagawa^1 , Peipei Wu^1 , Rachappa Balkunde^1 , Patrick Cunniff^1 , David Jackson1,2*Messenger RNAs (mRNAs) function as mobile signals for cell-to-cell communication in multicellular
organisms. The KNOTTED1 (KN1) homeodomain family transcription factors act non–cell autonomously
to control stem cell maintenance in plants through cell-to-cell movement of their proteins and
mRNAs through plasmodesmata; however, the mechanism of mRNA movement is largely unknown.
We show that cell-to-cell movement of a KN1 mRNA requires ribosomal RNA–processing protein 44A
(AtRRP44A), a subunit of the RNA exosome that processes or degrades diverse RNAs in eukaryotes.
AtRRP44A can interact with plasmodesmata and mediates the cell-to-cell trafficking of KN1 mRNA,
and genetic analysis indicates that AtRRP44A is required for the developmental functions of SHOOT
MERISTEMLESS, anArabidopsisKN1 homolog. Our findings suggest that AtRRP44A promotes
mRNA trafficking through plasmodesmata to control stem cell–dependent processes in plants.C
ell-to-cell communication in multicellu-
lar organisms promotes cell fate specifi-
cation and coordination of development.
As one way to transmit information be-
tween cells, plants selectively traffic tran-
scription factors through plasmodesmata, cell
wall–embedded channels that connect the cy-
toplasm of neighboring cells ( 1 – 3 ). The maize
KNOTTED1 (KN1) homeodomain transcrip-
tion factor was the first mobile protein found
to use this trafficking pathway ( 4 ). Previ-
ous studies have identified regulators of
KN1 protein trafficking ( 5 – 7 ); however, KN1
protein traffics with its mRNA ( 4 ). Selective
trafficking of mRNAs in plants is prevalent
( 8 – 12 ); however, the mechanism by which this
occurs through plasmodesmata has not been
addressed. Here, we identifyArabidopsisribo-
somal RNA–processing protein 44A (AtRRP44A)
as an essential factor for the cell-to-cell traf-
ficking of KN1 mRNA and show that AtRRP44A-
dependent mRNA trafficking is required for
cell-to-cell protein trafficking and stem cell
functions in plants.Isolation of KN1 trafficking mutants
We previously established a genetic screen
inArabidopsisto identify regulators of KN1
cell-to-cell trafficking by using a“trichome
rescue system”( 7 , 13 ). Trichomes are hairlike
extensions of the leaf epidermis. Their de-
velopment requires the cell-autonomous activ-
ity of GLABROUS1 (GL1), a MYB transcription
factor ( 14 ). In our system, a fusion protein of
green fluorescent protein (GFP), GL1, and
the KN1 C-terminal trafficking domain (KN1C)
is expressed in the mesophyll cell layers ofleaves of trichomelessgl1mutants by using
the Rubisco small subunit 2b promoter
(pRbcS::GFP~GL1~KN1C)( 7 ). Trafficking of
GFP~GL1~KN1Cto the epidermis rescues
trichome formation in this line; thus, trichome
number is an output for KN1 trafficking. In
an ethyl methanesulfonate (EMS) mutagenesis
screen of trichome rescue lines, we isolated two
mutants that lacked trichomes, which were
initially referred to asrb31-7andmk5-140
(Fig.1,AtoC).Consistentwiththelossof
trichomes, epidermal GFP~GL1~KN1Caccumu-
lation decreased significantly in the mutants
(Fig. 1, D to F) despite similar expression
compared with that of the parental control
trichome rescue lines in mesophyll cell layers
(Fig. 1, G to I). These observations suggest that
both mutants reduced the trafficking of GFP
~GL1~KN1Cfrom the mesophyll cell layers to
the epidermis. To investigate whether trichome
loss in the mutants was simply due to a re-
duction in transgene expression, we measured
GFP~GL1~KN1Cfluorescence in mesophyll cells
of the mutants. We found that it was ~50 to
70% of the level in the parental trichome
rescue lines (fig. S1A). However, this reduction
wasnotthecauseoftrichomelossbecause
plants hemizygous for the trichome rescue
transgene also had ~50% expression, and this
was sufficient for trichome rescue (fig. S1, A
and B). Thus, we confirmed that KN1 traf-
ficking was inhibited inrb31-7andmk5-140
mutants.KN1 trafficking mutants encode AtRRP44A
Bothrb31-7andmk5-140mutants behaved as
single recessive loci. We mapped them by se-
quencing M3 pools of mutants or nonmutant
siblings to ~44× coverage. Using the MutMap+
pipeline ( 15 ), we identified potentially causal
point mutations ofrb31-7andmk5-140with-
in the same gene, At2g17510 [guanine (G) to
adenine (A) and cytosine (C) to thymine (T),
which causes disruptive Cys^551 to Tyr and Pro^781SCIENCEscience.org 14 JANUARY 2022•VOL 375 ISSUE 6577 177
(^1) Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
11724, USA.^2 National Key Laboratory of Crop Genetic
Improvement, Huazhong Agricultural University, Wuhan
430070, P.R. China.
*Corresponding author. Email: [email protected]
†Present address: Bayer Crop Science LLC, Chesterfield, MO
63017, USA.
RESEARCH | RESEARCH ARTICLES