Abstract
Environmental cues profoundly modulate cell proliferation and cell elongation to inform and direct plant growth and development. External phosphate (Pi) limitation inhibits primary root growth in many plant species. However, the underlying Pi sensory mechanisms are unknown. Here we genetically uncouple two Pi sensing pathways in the root apex of Arabidopsis thaliana. First, the rapid inhibition of cell elongation in the transition zone is controlled by transcription factor STOP1, by its direct target, ALMT1, encoding a malate channel, and by ferroxidase LPR1, which together mediate Fe and peroxidase-dependent cell wall stiffening. Second, during the subsequent slow inhibition of cell proliferation in the apical meristem, which is mediated by LPR1-dependent, but largely STOP1–ALMT1-independent, Fe and callose accumulate in the stem cell niche, leading to meristem reduction. Our work uncovers STOP1 and ALMT1 as a signalling pathway of low Pi availability and exuded malate as an unexpected apoplastic inhibitor of root cell wall expansion.
Highlights
Environmental cues profoundly modulate cell proliferation and cell elongation to inform and direct plant growth and development
Much has been learned from LOW PHOSPHATE ROOT 1 (LPR1) and PHOSPHATE DEFICIENCY RESPONSE 2 (PDR2), which genetically interact and are expressed in cell type-specific but overlapping domains of the root apex, comprising the root apical meristem (RAM) and early EZ8,9,12
Together with root length and growth kinetics analysis, our results show that the absence of rapid inhibition of root growth of stop[1] and almt[1] under À Pi correlates with reduced accumulation of Fe and callose in the elongation zone (EZ), whereas the late root growth inhibition correlates with accumulation of Fe and callose in the stem cell niche (SCN) and reduced RAM size
Summary
Environmental cues profoundly modulate cell proliferation and cell elongation to inform and direct plant growth and development. The underlying mechanisms of root growth inhibition by low Pi availability remain largely unknown To address this problem at the cellular and molecular level, we chose the primary root of Arabidopsis thaliana seedlings as the experimental system because it displays a transparent and simple anatomical structure. Decades of laboratory work have shown that cells proliferate in the root apical meristem (RAM) in concentric layers (epidermis, cortex and endodermis surrounding the stele) These cell types originate in the stem cell niche (SCN), enclosing the quiescent centre (QC), divide as transit-amplifying cells before rapid and extensive cell expansion ensues in the elongation zone (EZ)[3,4] (Supplementary Fig. 1a). Callose deposition in the SCN obstructs cell-to-cell communication as demonstrated by impaired movement of SHORT-ROOT, a key transcription factor of root patterning and cell fate specification[4], which is followed by reduced stem cell maintenance and RAM activity[12]
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