Strigolactones affect phosphorus acquisition strategies in tomato plants

Abstract

Strigolactones (SLs) are plant hormones that modulate morphological, physiological and biochemical changes as part of the acclimation strategies to phosphorus (P) deficiency, but an in-depth description of their effects on tomato P-acquisition strategies under P shortage is missing. Therefore, in this study, we investigate how SLs impact on root exudation and P uptake, in qualitative and quantitative terms over time, in wild-type and SL-depleted tomato plants grown with or without P. Under P shortage, SL-depleted plants were unable to efficiently activate most mechanisms associated with the P starvation response (PSR), except for the up-regulation of P transporters and increased activity of P-solubilizing enzymes. The reduced SL biosynthesis had negative effects also under normal P provision, because plants overactivated high-affinity transporters and enzymatic activities (phytase, acidic phosphatase) to sustain elevated P uptake, at great carbon and nitrogen costs. A shift in the onset of PSR was also highlighted in these plants. We conclude that SLs are master kinetic regulators of the PSR in tomato and that their defective synthesis might lead both to suboptimal nutritional outcomes under P depletion and an unbalanced control of P uptake when P is available.

Biological Functions of Strigolactones and Their Crosstalk With Other Phytohormones

“…The key genes, triad IPS1-miR399-PHO2 and the high-affinity P transporter LePT2, were involved in the response of tomato plants to low P availability (Gamir et al, 2020). No matter growing with P or not, SL biosynthesis-deficient tomato mutant could not efficiently activate most mechanisms associated with the P starvation response compared with wild-type plants (Santoro et al, 2021).…”

Tomato plant responses induced by sparingly available inorganic and organic phosphorus forms are modulated by strigolactones

“…First-strand cDNA was synthesized from 500 ng of purified total RNA using the High-Capacity cDNA Reverse-Transcription Kit (Applied Biosystems, Monza, Italy) according to the manufacturer's instructions. The specific primer pairs are the same as reported in Santoro et al (2021). The quantitative reverse-transcriptase PCR (qRT-PCR) reactions were carried out in a StepOnePlus system (Applied Biosystems) using the SYBR Green (Applied Biosystems) method.…”

“…The involvement of SLs in the regulation of plant responses to P deficiency likely occurs through their crosstalk with other phytohormones, such as cytokinins, auxin and ethylene, thus highlighting a complex network of hormonal signals involved in response to P scarcity (Kapulnik et al 2011;Villaécija-Aguilar et al 2019). Recently, we have reported that SLs partly mediate several physiological and morphological changes triggered by P deficiency (Santoro et al 2020(Santoro et al , 2021. We have observed that SL-depleted tomato plants differ from wild-type (WT) controls at the level of root morphology, as many root traits were more severely affected at low P provision (80 μM) (Santoro et al 2020).…”

“…We have observed that SL-depleted tomato plants differ from wild-type (WT) controls at the level of root morphology, as many root traits were more severely affected at low P provision (80 μM) (Santoro et al 2020). This condition induced many P-deficiency responses in SL-depleted plants, which WT plants only adopted under harsh P stress conditions, including extensive cell and tissue disorganization at the root tip (Santoro et al 2020(Santoro et al , 2021. The enhanced P uptake, expression of PHT genes and root enzymatic activity observed in SL-depleted plants compared to WT plants may be related to an altered perception of exogenous P and/or of endogenous P levels.…”

“…The enhanced P uptake, expression of PHT genes and root enzymatic activity observed in SL-depleted plants compared to WT plants may be related to an altered perception of exogenous P and/or of endogenous P levels. On the other hand, some responses such as root acidification in response to low P were initially delayed and impaired in the absence of SLs (Santoro et al 2021). The role of SLs in the ability of tomato plants to access different forms of sparingly available P sources, such as dissolved organic P or precipitated metal-P systems, is however still largely unknown.…”