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18th International Symposium on Iron Nutrition and Interaction in Plants
Madrid – May 30-June 3 2016
ROLE OF IRON IN ROOT PHOSPHATE SENSING
Jens Müller, Marcus Heisters, Theresa Toev, Ranju Chutia, Jörg Ziegler, and Steffen Abel*
Leibniz Institute of Plant Biochemistry, Department of Molecular Signal Processing, Halle (Saale), Germany
*corresponding author email address
Plant root development is highly responsive to numerous edaphic cues. The mineral nutrient inorganic
phosphate (Pi) and its derivative P-anhydrides constitute major nodes in bioenergetics and metabolism. Pi
deprivation directly impacts plant performance; however, limited Pi bioavailability is pervasive in soils and
caused by complex chemistries involving iron (Fe) and other metals, particularly with increasing soil depth. To
cope with Pi shortage, plants activate a set of coordinated biochemical and developmental responses that
enhance Pi recycling and Pi acquisition by reprogramming metabolism and redesigning root system
architecture. Pi limitation stimulates formation of a shallow root system by attenuating primary root extension
and promoting lateral root development (also known as topsoil foraging). Such changes in root development
are informed by local Pi supply, and previous studies suggested that Pi sensing at the root apex is modified
by external Fe availability (see Abel 2011).
To elucidate root Pi sensing, we characterized two functionally interacting genes in Arabidopsis thaliana, PDR2
(PHOSPHATE DEFICIENCY RESPONSE2) and LPR1 (LOW PHOSPHATE ROOT1) as well as their loss-offunction alleles that cause a hypersensitive (pdr2) and insensitive (lpr1) primary root growth response to low
Pi, respectively. Using the two epistatic mutants and the wild-type as a reference, we conducted a series of
experiments to compare in roots their Pi-responsive cell biology (Ticconi et al., 2009; Müller et al. 2015), their
exo-metabolome (Ziegler et al. 2016) as well as their transcriptome and proteome (Müller et al. 2016), which
all support a critical role of external Fe for mediating the local response of root meristems to Pi availability.
PDR2 codes for the single P5-type ATPase of unknown transport specificity (AtP5A), which is targeted to the
ER and likely controls LPR1 biogenesis. LPR1 encodes a cell wall-localized multicopper oxidase, which we
demonstrated to express ferroxidase activity. We present a first structure-function analysis of a plant
ferroxidase (LPR1). The expression domains of LPR1 and PDR2 overlap in the root meristem; however, LPR1
expression determines the sites of apoplastic Fe, ROS and callose accumulation, which interfere with cell-tocell communication in the root stem cell niche and promote accelerated cell differentiation followed by root
growth inhibition when Pi is limiting. As expected, a genetic screen for pdr2 suppressors identified LPR1, but
also a transporter of organic acids, which are known to function as Fe chelators. We developed a hydroponic
cultivation system to analyze and to compare by non-targeted metabolite profiling semi-polar compounds in
root exudates of Pi-replete and Pi-starved wild-type, pdr2 and lpr1 seedlings. Our data uncovered a role for
exuded coumarins as potential Fe chelators and for accelerated lignification during the local response to Pi
limitation. Similarly, genome-wide transcriptome and proteome analysis of the three genotypes in response to
Pi deficiency revealed overrepresentation of genes and proteins that are involved in the regulation of Fe
homeostasis, ROS formation and cell wall remodeling. Additional experiments support the hypothesis that
IRT1-independent Fe uptake by root tips and apoplastic Fe redistribution, but not intracellular Fe uptake and
Fe storage, control Pi-dependent cell wall modification and root growth modulation. Since Pi is the predominant
nutrient controlling primary root length, our complementary studies (cell biology, metabolite and comparative
gene expression profiling) provide a framework of how the relative abundance of Pi and Fe in soil shape root
system architecture.
Keywords: Phosphate-iron interactions, ferroxidase activity, meristem maintenance, root development
REFERENCES: Abel (2011) 14:303-309; Ticconi et al. (2009) PNAS 106:14174-14179; Müller et al. (2015)
Dev Cell 33:216-230; Ziegler et al. (2016) 67:1421-1432; Müller et al. (2016) BMC Plant Biol (in press).
ACKNOWLEDGEMENT: Research at the Leibniz Institute of Plant Biochemistry is supported by institutional
core funding provided by the state of Saxony-Anhalt and the federal Republic of Germany.
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