Don’t Go Grocery Shopping When Hungry! Systemic Signaling in Zinc Homeostasis

Going grocery-shopping on an empty stomach is a bad idea. You’re bound to make poor decisions, not based on nutritional content of the food but based on temporary cravings that will leave you asking for more later. Plants face this nutritional puzzle every day, since they eat where they shop, and shop while they eat.

Roots are the sole entry for nutrients, and must coordinate uptake to sustain optimal growth while preventing accumulation to toxic levels. Roots therefore need to balance their needs with those of leaves and shoots, which involves long-distance, or systemic, signals. So far, local and long-distance control mechanisms had been described for iron and inorganic phosphate, and new work by Sinclair and colleagues (Sinclair et al., 2018) adds the micronutrient zinc to the list.

The authors used a genetic trick to dissect the relative contributions of local and systemic signals in zinc homeostasis: the hma2 hma4 double mutant, which lacks two HEAVY METAL ATPASEs thought to send zinc from the root to the shoot. Without them, assimilated zinc stays in the root and fools the tissue into thinking it has more than enough of the micronutrient for growth. Meanwhile, hma2 hma4 shoots do not get enough zinc and experience zinc deficiency, as shown by high expression of the zinc transporters ZIP4 and ZIP9, members of the ZRT/IRT-like Protein family (see Figure).

Roots of hma2 hma4 plants receive a shoot-derived systemic zinc deficiency signal, although the local physiological status is zinc-replete. A comparison of transcriptomes from wild-type and mutant roots revealed a number of candidate target genes in roots of the shoot-derived systemic zinc signal. One of these genes was found to encode METAL TRANSPORT/TOLERANCE PROTEIN 2 (MTP2), another predicted zinc transporter.

ZIP4, ZIP9, MTP2, and HMA2 are highly induced in roots under low zinc conditions. A long-distance signal, sent from the shoot to the root, should adapt to the shoot zinc status, for example when spraying a zinc solution onto leaves. Indeed, MTP2 and HMA2 expression (although not ZIP4 or HMA4) decreased in the roots of zinc-deficient plants whose leaves were sprayed with zinc. In addition, ZIP4 and MTP2 expression followed distinct kinetics in zinc-deficient plants watered with extra zinc: ZIP4 expression was quickly repressed, while MTP2 expression stayed high longer, presumably until root-assimilated zinc reached the shoot and dialed down the systemic signal.

What is the role of MTP2 in zinc homeostasis? MTP2 expression is restricted to roots and siliques, so it should not generate or relay the signal itself. The protein is a functional zinc transporter, as its heterologous expression rescues a yeast mutant affected in intracellular zinc sequestration. MTP2 co-localizes with an aquaporin that resides in the Endoplasmic Reticulum (ER) membrane, suggesting that MTP2 transports zinc into the ER lumen, which is shared between adjacent roots cells. This ER route may deliver zinc efficiently to the inner root layer, bringing zinc closer to the vasculature. The plasma membrane zinc efflux pump HMA2 then takes over and loads the apoplastic xylem with zinc for eventual delivery to the shoot (see Figure).

Reverse genetics confirmed the model above: mtp2 and hma2 mutants were smaller than wild-type and accumulated less zinc in their shoots (but not in roots) only when grown in low zinc conditions. These phenotypes were even more pronounced in the mtp2 hma2 double mutant, arguing for a shared role for MTP2 and HMA2 in shootward zinc mobilization.

In this elegant study, Sinclair and colleagues thus demonstrate the existence of a systemic zinc signal that enhances the translocation of zinc to the shoot. The nature of the signal is still unknown, but the transcriptome data of shoots yielded more candidates to investigate, which could contribute to solving the problem of zinc limitation for crop production (Alloway, 2008).

REFERENCES

Alloway, B.J. (2008). Zinc in Soils and Crop Nutrition. (Brussels, Belgium, Paris, France: International Zinc Association, International Fertilizer Industry Association).

Sinclair, S.A., Senger, T., Talke, I.N., Cobbett, C.S. ,Haydon, M.J. and Kraemer, U.  (2018) Systemic upregulation of MTP2- and HMA2-mediated Zn partitioning to the shoot supplements local Zn deficiency responses of Arabidopsis. Plant Cell 10.1105/tpc.18.00207