Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate

Abstract

Low phosphate (Pi) availability constrains plant development and seed production in both natural and agricultural ecosystems. When Pi is scarce, modifications of root system architecture (RSA) enhance the soil exploration ability of the plant and lead to an increase in Pi uptake. In Arabidopsis, an iron-dependent mechanism reprograms primary root growth in response to low Pi availability. This program is activated upon contact of the root tip with low-Pi media and induces premature cell differentiation and the arrest of mitotic activity in the root apical meristem, resulting in a short-root phenotype. However, the mechanisms that regulate the primary root response to Pi-limiting conditions remain largely unknown. Here we report on the isolation and characterization of two low-Pi insensitive mutants (lpi5 and lpi6), which have a long-root phenotype when grown in low-Pi media. Cellular, genomic, and transcriptomic analysis of low-Pi insensitive mutants revealed that the genes previously shown to underlie Arabidopsis Al tolerance via root malate exudation, known as SENSITIVE TO PROTON RHIZOTOXICITY (STOP1) and ALUMINUM ACTIVATED MALATE TRANSPORTER 1 (ALMT1), represent a critical checkpoint in the root developmental response to Pi starvation in Arabidopsis thaliana. Our results also show that exogenous malate can rescue the long-root phenotype of lpi5 and lpi6. Malate exudation is required for the accumulation of Fe in the apoplast of meristematic cells, triggering the differentiation of meristematic cells in response to Pi deprivation.

Role of cis‐zeatin in root responses to phosphate starvation

“…To estimate the effect of root illumination in this molecular response, we compared our data with those reported by Mora‐Macias et al . (), in which roots were grown in the presence of light. We found that only 29% of the upregulated transcripts and 22% of the downregulated transcripts were common between both datasets (Fig.…”

“…Phosphate starvation has a significant impact on global gene expression (Misson et al ., ; Bustos et al ., ; Woo et al ., ; Secco & Whelan, ; Mora‐Macias et al ., ). These analyses, together with genetic studies (Rubio et al ., ; Catarecha et al ., ; Ticconi et al ., ; Nussaume et al ., ; Gamuyao et al ., ; Wang et al ., ; Ruan et al ., ), have shed light on the molecular mechanisms that regulate the PSR.…”

The genetics underlying natural variation of plant–plant interactions, a beloved but forgotten member of the family of biotic interactions

“…Upon nitrogen depletion, roots secrete small C‐terminally Encoded Peptides (CEPs) which are translocated to the shoot and are perceived by leucine‐rich repeat receptor kinases (LRR‐RKs) to activate nitrate transporters such as NRT1.1 (Sun et al ., for a review; Tabata et al ., ). Recent additions to the list of foraging regulators include STOP1 and ALMT1 that mediate phosphate‐induced root remodeling through malate exudation (Balzergue et al ., ; Mora‐Macias et al ., ). Depending on the source of phosphate available in the soil, the grass Deschampsia cespitosa produces more biomass when grown with a different grass species than with conspecifics, suggesting that nutrient availability regulates plant competition (Ahmad‐Ramli et al ., ).…”

Low phosphate represses histone deacetylase complex1 to regulate root system architecture remodeling in Arabidopsis

“…PDR2 encodes a P5-type ATPase, whereas LPR1/2 is a ferroxidase, which enables ROS generation and callose deposition in both the apoplast surrounding the stem cell niche (SCN) of the root apical meristem (RAM) and the root transition zone. Recently, it was also reported that mutants of other Al tolerance genes, stop1 and almt1, are both insensitive to Pi deficiency in terms of primary root growth inhibition (Balzergue et al, 2017;Mora-Mac ıas et al, 2017). The hsp10 allele is a loss-of-function allele of ALUMINUM SENSITIVE3 (ALS3), which encodes a half-size ABC transporter involved in Al resistance (Xu et al, 2019).…”