The Art of Self-Control - Autoregulation of Plant-Microbe Symbioses

Abstract

Plants interact with diverse microbes including those that result in nutrient-acquiring symbioses. In order to balance the energy cost with the benefit gained, plants employ a systemic negative feedback loop to control the formation of these symbioses. This is particularly well-understood in nodulation, the symbiosis between legumes and nitrogen-fixing rhizobia, and is known as autoregulation of nodulation (AON). However, much less is understood about the autoregulation of the ancient arbuscular mycorrhizal symbioses that form between Glomeromycota fungi and the majority of land plants. Elegant physiological studies in legumes have indicated there is at least some overlap in the genes and signals that regulate these two symbioses but there are major gaps in our understanding. In this paper we examine the hypothesis that the autoregulation of mycorrhizae (AOM) pathway shares some elements with AON but that there are also some important differences. By reviewing the current knowledge of the AON pathway, we have identified important directions for future AOM studies. We also provide the first genetic evidence that CLV2 (an important element of the AON pathway) influences mycorrhizal development in a non-legume, tomato and review the interaction of the autoregulation pathway with plant hormones and nutrient status. Finally, we discuss whether autoregulation may play a role in the relationships plants form with other microbes.

Keywords: CLAVATA; CLE peptide; arbuscular mycorrhizae; autoregulation; nodulation; tomato.

FIGURE 1

Proteins and signals that act in the shoot and/or root to autoregulate nodulation and mycorrhizal symbioses. Flat-ended lines indicate a negative influence, while arrows indicate a positive influence. Question marks and dotted lines indicate untested elements. CK, cytokinin; N, nitrogen; P, phosphorous; Rh, rhizobial; Myc, mycorrhizal; arb, arabinosylated.

FIGURE 2

Mycorrhizal colonization in tomato wild type (WT, M82) and clv2-2 lines. (A) Percentage of the root colonized by all fungal structures and arbuscules. n = 12, values are means + SE t-tests were performed for each parameter, ^∗P < 0.05, ^∗∗P < 0.01. (B) Photograph of a typical length of colonized root (scale bar = 100 μm) after staining fungal structures (blue). Tomato seeds were germinated in potting mix for 2 weeks and 12 equal sized seedlings of each genotype were selected and transplanted to 2 L pots. The pots were premixed with vermiculite and gravel (1:1) plus mycorrhizal inoculum (1/5 volume of corn roots colonized with Rhizophagus irregularis and associated potting medium) and topped with vermiculite. The seedlings were grown in a glasshouse with the following condition: 18 h photoperiod, 25°C day/20°C night. Plants were nutriented three times a week with modified Long Ashton solution (5 mM N and 0.5 mM P) (Hewitt, 1966). Plants were harvested 6 weeks after transplanting. The root was cut into 1 to 1.5 cm segments and stained using the ink and vinegar method (Vierheilig et al., 1998). 25 root segments were selected per plant and mycorrhizal colonization scored using the intersect scoring method (McGonigle et al., 1990). Blind labeling was used to avoid any potential bias during the scoring process.