A phosphate starvation response‐regulated receptor‐like kinase, OsADK1, is required for mycorrhizal symbiosis and phosphate starvation responses

Abstract

Most land plants associate with arbuscular mycorrhizal (AM) fungi to secure mineral nutrient acquisition, especially that of phosphorus. A phosphate starvation response (PHR)centered network regulates AM symbiosis.Here, we identified 520 direct target genes for the rice transcription factor OsPHR1/2/3 during AM symbiosis using transcriptome deep sequencing and DNA affinity purification sequencing. These genes were involved in strigolactone biosynthesis, transcriptional reprogramming, and bidirectional nutrient exchange.Moreover, we identified the receptor-like kinase, Arbuscule Development Kinase 1 (OsADK1), as a new target of OsPHR1/2/3. Electrophoretic mobility shift assays and transactivation assays showed that OsPHR2 can bind directly to the P1BS elements within the OsADK1 promoter to activate its transcription. OsADK1 appeared to be required for mycorrhizal colonization and arbuscule development. In addition, hydroponic experiments suggested that OsADK1 may be involved in plant Pi starvation responses.Our findings validate a role for OsPHR1/2/3 as master regulators of mycorrhizal-related genes involved in various stages of symbiosis, and uncover a new RLK involved in AM symbiosis and plant Pi starvation responses.

The good, the bad, and the phosphate: regulation of beneficial and detrimental plant–microbe interactions by the plant phosphate status

“…Among them are SL biosynthesis genes and LysM‐RLKs involved in precontact signaling, common symbiosis genes required for fungal cell entry such as SYMBIOSIS RECEPTOR KINASE ( SYMRK ), CALCIUM and CALMODULIN DEPENDENT KINASE (CCaMK ) and CYCLOPS and genes encoding nutrient transporters, which operate in nutrient exchange at the peri‐arbuscular membrane (Fig. 2a; Das et al ., 2022; Shi et al ., 2022). For the common symbiosis genes SYMRK, CCaMK, and CYCLOPS, this was confirmed in the phr1a mutant of the model legume and dicotyledon Lotus japonicus (Das et al ., 2022).…”

Re-engineering a lost trait:IPD3, a master regulator of arbuscular mycorrhizal symbiosis, affects genes for immunity and metabolism of non-host Arabidopsis when restored long after its evolutionary loss

“…Recently, significant portions of the AMF genetic network were revealed to be under control of the phosphate-stress-responsive PHR-SPX system, which is conserved in Arabidopsis (Shi et al, 2021; Shi et al, 2022). In Arabidopsis , PHR also regulates the microbiome by reducing plant defenses when phosphate is low, resulting in recruitment of beneficial microbes (Finkel et al 2019, Martin-Rivilla et al 2019, Castrillo et al 2017,Cho, Kang, and Kim 2013; Kotchoni and Gachomo 2006; Dangl 1998).…”

Microbe‐dependent and independent nitrogen and phosphate acquisition and regulation in plants

“…Interestingly, Shi et al . (2022), showed that the expression of the MtKIN3 homolog OsARK1 is regulated by PHRs in rice, further indicating crosstalk between nitrogen and Pi signaling.…”

“…Recent studies in M. truncatula showed that kin3 mutants display a much lower mycorrhizal infection rate than the wild-type under high-nitrogen conditions, while root colonization under low-nitrogen conditions was not affected, indicating that it plays a role in adjusting the symbiotic response according to soil nitrogen levels (Irving et al, 2022). Interestingly, Shi et al (2022), showed that the expression of the MtKIN3 homolog OsARK1 is regulated by PHRs in rice, further indicating crosstalk between nitrogen and Pi signaling.…”

“…PHRs appear to be global regulators that are involved in both the early and late stages of the mycorrhizal symbiosis. DAP‐Seq and ChIP‐Seq were used to find PHR2 target regions, and demonstrated that OsPHR2‐binding peaks were present in the promoter regions of AM symbiosis‐related genes (Das et al ., 2022; Shi et al ., 2022). PHR targets include the strigolactone biosynthesis genes, CAROTENOID CLEAVAGE DIOXYGENASE 7 and 8a ( CCD7 and CCD8a ), which are required to activate AM fungal metabolism and branching, and the nutrient exchange‐related genes, WRINKLED 5a ( WRI5a ) and PT11 , and the root epidermal surface receptors, CERK1 and SYMBIOSIS RECEPTOR‐LIKE KINASE ( SYMRK ), which are involved in the perception of fungal signals.…”