Novel Insights Into the Hyperaccumulation Syndrome in Pycnandra (Sapotaceae).

Sandrine Isnard,Vidiro Gei,Antony Van Der Ent,Adrian L D Paul,Guillaume Echevarria,Jérôme Munzinger,Laurent L’Huillier,Peter D Erskine,Bruno Fogliani,Tanguy Jaffré

doi:10.3389/fpls.2020.559059

Abstract

The discovery of nickel hyperaccumulation, in Pycnandra acuminata, was the start of a global quest in this fascinating phenomenon. Despite recent advances in the physiology and molecular genetics of hyperaccumulation, the mechanisms and tolerance of Ni accumulation in the most extreme example reported to date, P. acuminata, remains enigmatic. We conducted a hydroponic experiment to establish Ni tolerance levels and translocation patterns in roots and shoots of P. acuminata, and analyzed elemental partitioning to gain insights into Ni regulation. We combined a phylogeny and foliar Ni concentrations to assess the incidence of hyperaccumulation within the genus Pycnandra. Hydroponic dosing experiments revealed that P. acuminata can resist extreme Ni concentrations in solution (up to 3,000 µM), and dosing at 100 µM Ni was beneficial to growth. All plant parts were highly enriched in Ni, but the latex had extreme Ni concentrations (124,000 µg g−1). Hyperaccumulation evolved independently in only two subgenera and five species of the genus Pycnandra. The extremely high level of Ni tolerance is posited to derive from the unique properties of laticifers. The evolutionary and ecological significance of Ni hyperaccumulation in Pycnandra is discussed in light of these findings. We suggest that Ni-rich laticifers might be more widespread in the plant kingdom and that more investigation is warranted.

Highlights

The seminal report by Jaffré et al (1976) on the nickel (Ni)-rich latex of Pycnandra acuminata introduced the term “hyperaccumulator” and gave rise to a new field of research (Jaffré et al, 1976; Jaffré et al, 2018)
Pycnandra acuminata plants were cultivated in hydroponic solutions for 6 months and growth, biomass production, and elemental concentrations in roots and shoots were analyzed
No significant difference in Ni concentration between the shoot compartments were found in the other treatments, except in the 3,000 μM Ni treatment, where Ni accumulates at significantly higher concentrations in the apical shoot (11,200 μg g−1 vs. 8,700 μg g−1) (Table 1)

Summary

Introduction

The seminal report by Jaffré et al (1976) on the nickel (Ni)-rich latex of Pycnandra acuminata (previously Sebertia acuminata; Sapotaceae) introduced the term “hyperaccumulator” and gave rise to a new field of research (Jaffré et al, 1976; Jaffré et al, 2018). While most plants only contain ≤10 μg g−1 of Ni in their tissues, Ni-hyperaccumulators are Extreme Nickel Tolerance in Pycnandra capable of accumulating ≥ 1,000 μg g−1 of Ni in their tissues (Brooks et al, 1977). One key function of Ni is as an essential component of urease, an enzyme which catalyzes urea hydrolysis for the release of ammonia (Gerendás et al, 1999; Taiz and Zeiger, 2006). This activity contributes to the recycling of endogenous nitrogen for plant growth (Gerendás et al, 1999). The biomass production of hyperaccumulators (e.g. Alyssum bertolonii, Noccaea goesingense, Berkheya coddii) remains unaffected by Ni concentrations of up to several hundred μM in the hydroponic solution (Gabbrielli et al, 1991; Krämer et al, 1997; Robinson et al, 2003)

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Conclusion