K+ Nutrition Exchange in the Serendipita-Arabidopsis Symbiosis: Study of the Fungal K+ Transporters Involved

Abstract

There is mounting evidence that the root-colonizing endosymbiotic fungus Serendipita indica improves plant growth. The beneficial effects have been observed when plants are growing in optimal conditions or under nutritionally deficient soils (e.g., phosphate poor soil) or exposed to stressful environmental conditions such as drought or salinity. However, until now its role in the nutrition of other plant essential macronutrient, such as K+, has not been fully clarified. Here, we study the role of the fungus in the K+ nutrition of Arabidopsis thaliana plants, during growth under K+ limiting conditions. As a first step, we studied the high-affinity K+ uptake of the plant and fungus when growing separately and in symbiosis. In the search for putative fungal actors involved in K+ nutrition, we also have cloned and functionally characterized the K+ transporters of S. indica SiHAK1, SiTRK1, SiTRK2, and SiTOK1, among which it has been shown that SiHAK1 is the main transporter involved in the K+ uptake in the high affinity range of concentrations. In addition, a gene expression study of these transporters and other candidates that could participate in the K+ homeostasis of the fungus has been carried out. The results indicated that, contrary to what happens with P nutrition, S. indica seems not to improve neither the growth nor the plant K+ reserves during K+ starvation. Instead, this nutritionally restrictive condition favored fungal colonization, suggesting that the fungus obtains the greatest benefit in K+ supply during symbiosis.

The calcium sensor CBL7 is required for Serendipita indica‐induced growth stimulation in Arabidopsis thaliana, controlling defense against the endophyte and K+ homoeostasis in the symbiosis

“…Potassium depletion in the shoot could trigger the induction of HAK5 in cbl7 , as multiple independent studies demonstrated that HAK5 is induced under K + starvation (Ahn et al, 2004 ; Armengaud et al, 2004 ; Gierth et al, 2005 ; Shin & Schachtman, 2004 ). A recent study demonstrated the induction of HAK5 in the host plant as a general consequence of the symbiotic interaction (Conchillo et al, 2021 ), which would also explain why we found HAK5 under the consistently induced genes in wild‐type plants (Figure 1 ). Furthermore, the latter study demonstrated that the inoculation of Arabidopsis with S. indica does not improve the K + nutrition of the host plant under K + limiting conditions.…”

“…As shown in Figure 4 , the potassium content of the cbl7‐2 roots grown at 0 mM KCl was similar to that of the Col‐3 control plants. However, the previously described decrease in K + contents in response to the inoculation with S. indica (Conchillo et al, 2021 ) was only observed in control plants, but not in cbl7‐2 . Interestingly, the K + level in the shoots of cbl7‐2 plants was significantly lower than in the mock‐treated wild type, equal to the level observed for Col‐3 treated with the fungus.…”

“…The analysis of endogenous cation contents of infected and control plants was performed according to Conchillo et al ( 2021 ) in fractions of root and shoot samples. In brief, the fungi were first K + depleted buy inoculating 100 ml AP medium containing 1 mM K + with 1.5 × 10 3 of the corresponding spores and incubating it for 1 week at 28°C.…”

Molecular mechanisms of Piriformospora indica mediated growth promotion in plants

“…SiHAK1, SiTRK1, SiTRK2 and SiTOK1 . 31 Nonetheless, in the low K + condition P. indica did not promote the growth of Arabidopsis. Surprisingly, under the condition of K + deficiency, P. indica reduces overall K + accumulation in the host plant while improving its own growth by expressing its own K + transporter gene SiHAK1 .…”

“…P. indica alters multiple phytohormonal regulated pathways during colonization, e.g. jasmonate-regulated secondary metabolite, glucosinolate pathway during early stages of interaction, 31 rapid increase in auxin levels during early recognition of the host, which is important for reprogramming the root development, 33 - elevated level of auxins in Arabidopsis roots, 5 and P. indica itself also produces IAA in the liquid culture. 34 In a recent study, it has been elucidated that P. indica employs putrescine for plant’s growth promotion.…”