Characterization of low phosphorus insensitive Mutants Reveals a Crosstalk between Low Phosphorus-Induced Determinate Root Development and the Activation of Genes Involved in the Adaptation of Arabidopsis to Phosphorus Deficiency

Abstract

Low phosphorus (P) availability is one of the most limiting factors for plant productivity in many natural and agricultural ecosystems. Plants display a wide range of adaptive responses to cope with low P stress, which generally serve to enhance P availability in the soil and to increase its uptake by roots. In Arabidopsis (Arabidopsis thaliana), primary root growth inhibition and increased lateral root formation have been reported to occur in response to P limitation. To gain knowledge of the genetic mechanisms that regulate root architectural responses to P availability, we designed a screen for identifying Arabidopsis mutants that fail to arrest primary root growth when grown under low P conditions. Eleven low phosphorus insensitive (lpi) mutants that define at least four different complementation groups involved in primary root growth responses to P availability were identified. The lpi mutants do not show the typical determinate developmental program induced by P stress in the primary root. Other root developmental aspects of the low P rescue system, including increased root hair elongation and anthocyanin accumulation, remained unaltered in lpi mutants. In addition to the insensitivity of primary root growth inhibition, when subjected to P deprivation, lpi mutants show a reduced induction in the expression of several genes involved in the P starvation rescue system (PHOSPHATE TRANSPORTER 1 and 2, PURPLE ACID PHOSPHATASE 1, ACID PHOS-PHATASE 5, and INDUCED BY PHOSPHATE STARVATION 1). Our results provide genetic support for the role of P as an important signal for postembryonic root development and root meristem maintenance and show a crosstalk in developmental and biochemical responses to P deprivation.Phosphorus (P) is one of the most important nutrients for plant growth and development. P plays a myriad of essential biological functions as a structural element in phospholipids and nucleic acids, in energy metabolism, in the regulation of enzymatic activities, and in signal transduction cascades (Raghothama, 1999;Rausch and Bucher, 2002). Although the total content of P in the soil may be high, its bioavailability is generally very low due to mineralization and fixation processes (Hinsinger, 2001). Thus, low P availability is one of the prime limiting factors for plant growth and development in many ecosystems and a major constraint for agricultural productivity in alkaline and acid soils (Ló pez- Bucio et al., 2000).Plants have evolved a wide range of adaptive strategies to adapt to P deficiency and improve P mobilization and uptake from the soil (Raghothama, 1999), including an increase in the synthesis and secretion of organic acids, which enhance the solubilization of P from insoluble inorganic compounds (Jones, 1998); an increase in the production of enzymes such as acid phosphatases and nucleases that release P from soil organic sources (Nü rnberger et al., 1990; Löffler et al., 1992;Duff et al., 1994;Chen et al., 2000); an enhanced expression of highaffinity P transporters to optimize P uptake from ...

ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability

“…In Arabidopsis, Pi limitation attenuates primary root growth and stimulates lateral root formation, which is thought to maximize Pi acquisition in the topsoil (8,9). A genetic approach to dissect Pi sensing identified Arabidopsis mutants (10,11) and accessions (12,13) with altered sensitivity to the inhibitory effect of Pi deprivation on primary root growth. Characterization of a major quantitative trait locus for root length, low phosphate root 1 (lpr1), revealed a role for multicopper oxidases (LPR1, LPR2) in Pi sensing at the root tip (13,14).…”

Altered Expression of a Malate-Permeable Anion Channel, OsALMT4, Disrupts Mineral Nutrition

“…AtALMT1 is a member of the ALMT family in Arabidopsis, which encodes a malate-permeable anion channel. AtALMT1 is induced under conditions of low P, and Mora-Macías et al (2017) found that atalmt1 mutants did not show the usual inhibition of primary root growth displayed by wild-type plants when they grew into medium with low P levels (Sánchez-Calderón et al, 2006). The authors proposed that, in wild-type plants, malate release via AtALMT1 interacts with iron in the medium and causes Fe 3+ to aggregate in the apoplast of the root apices.…”

A role for redox factors in shaping root architecture under Phosphorus deficiency

“…Cells of the quiescent centre (QC) that accumulate high auxin levels are characterized by the oxidized status of ascorbate and glutathione and the overproduction of ROS. On the other hand, in rapidly dividing cells of the proximal meristem, the reduced status of ascorbate A role for redox factors in shaping root architecture under phosphorus deficiency Jarosław Tyburski,* Kamila Dunajska and Andrzej Tretyn Department of Biotechnology; Institute of General and Molecular Biology; Nicolaus Copernicus University; Torun, Poland articLe addendum articLe addendum primary root growth in P-deficient plants, 5 are accompanied by an elimination of the ROS distribution pattern typical for growing roots. This includes a decrease in ROS level in the elongation zone (Fig.…”

“…In a manner similar to the primary root tip, cell differentiation in older lateral roots occurs within the apical root meristem, which is followed by an arrest in lateral root elongation. 4,5 Besides the reduction in cell division rate, low P treatments inhibit cell growth in root elongation zone. 5,6 Promotion of lateral root development and the arrest of cell divisions in the apices of roots of P-starved plants results from changes in auxin transport and/or sensitivity.…”

“…4,5 Besides the reduction in cell division rate, low P treatments inhibit cell growth in root elongation zone. 5,6 Promotion of lateral root development and the arrest of cell divisions in the apices of roots of P-starved plants results from changes in auxin transport and/or sensitivity. 3,4 However, the processes affected by P-deficiency, namely, cell division and elongation are to a large extent, regulated by redox factors like radical oxygen species (ROS) or ascorbate.…”