A king and vassals’ tale: ecological cooperation in a marine clonal plant under energy shortage

Author Miriam Ruocco offers an insight into her paper A king and vassals’ tale: Molecular signatures of clonal integration in Posidonia oceanica under chronic light shortage. Find out more about the work, including why seagrass can be similar to a beehive!

While it is easy for us to think about eusociality and ecological cooperation in insects such as honeybees or ants, plants are generally considered to be passive organisms; incapable of any kind of  independent action or social behaviour (Mancuso & Viola, 2015). In truth, plants represent probably the best example of social intelligence among living organisms, and display extraordinary capabilities to solve problems, communicate, and understand their surroundings. This challenges the common idea of them as “unthinking” organisms (Mancuso & Viola, 2015).

A Posidonia oceanica meadow. Photo: Javier Ferrer

Such social capabilities are especially evident in clonal plants, which are modular organisms composed of repetitive and independent units, resulting from non-sexual reproduction. All these genetically-identical ramets are physically connected through horizontal structures like rhizomes or stolons that allow for the translocation of resources such as water and nutrients, as well as hormones, photosynthates and secondary metabolites. This form of cooperation, called clonal or physiological integration, permits the plant clone to cope with heterogeneities of the environment and to work as a macro-organism. For example, donor ramets situated in favourable microsites (those with abundant resource supply) can help resource-poor or otherwise adversely-placed ramets to alleviate their shortages and/or to tolerate abiotic and biotic stressors (Liu et al., 2016). Clonal integration can buffer against environmental changes and thus supports species persistence. However, the molecular signals that regulate this phenomenon are not completely unravelled.

Our indoor mesocosm facility for seagrass cultivation at Stazione Zoologica Anton Dohrn of Naples. Photo: Miriam Ruocco

In our recent paper, we shed first light on the molecular and physiological mechanisms underlying clonal integration in a marine flowering plant. Seagrasses are rhizomatous plants sharing a similar morphology to that of terrestrial monocotyledons, with the ability to reproduce either clonally or sexually. Seagrasses are of key ecological importance and represent one of the most productive components of benthic coastal ecosystems. In the Mediterranean Sea, the endemic species Posidonia oceanica forms extensive meadows that are among the most valuable marine ecosystems on Earth; fulfilling important ecosystem services from carbon sequestration to coastal protection and maintenance of fisheries. P. oceanica possess two types of ramets; namely, apical (horizontal, terminal) and vertical ramets. Clonal integration has been demonstrated in seagrasses in the form of nitrogen and carbon translocation among neighbouring ramets (Marbà et al., 2002). Photosynthates and nutrients can be re-allocated within seagrasses mainly toward organs with high metabolic activity, including growing leaves, flowering shoots and, remarkably, apical shoots, thus resulting in an enhanced clone growth and meadow spreading.

We analysed the differential behaviour of these two ramet types at molecular, photo-physiological and morphological levels, under an exposure to chronic light shortage (80% diminishing light irradiance), by means of a 40 day-long mesocosm experiment.

Schematic representation of main responses of vertical and apical shoots in P. oceanica under light shortage. Overall signatures of photo-physiological, morphological and molecular variables are outlined in the grey boxes. Specific transcriptomic rearrangements are synthetized in round brackets. ΔF/Fm’: photosynthetic performance, TNC: Total non-structural carbohydrates, 5-mC%: % DNA methylation level, DEGs: differentially expressed genes, GO-BPs: Gene-Ontology enriched biological processes. Diagram: Miriam Ruocco

Our multi-level analysis demonstrated a high level of specialisation of the different ramets within seagrass clones and a “division of labour” under adverse conditions. It appears that vertical shoots (that we re-named “the vassals”), do most of the job, especially in terms of resource (e.g. sugars) provided to the clone. They suffered from sugar starvation and showed a clear cellular stress response in terms of protein refolding and induction of DNA repair mechanisms. Apical shoots (that we re-named “the kings”) stopped growing and kept only few important processes activated, according to an “energy-saving” strategy. The communication between the shoot types was based on hormone release, probably auxin or cytokinins, as related functions were activated in both shoot types, particularly in apical ones.

Ultimately, vertical shoots appear to sacrifice themselves to protect the apical ones, those responsible for colonisation and population maintenance through clonal extension, similar to honeybee workers that sacrifice themselves to protect the hive.

Miriam Ruocco Stazione Zoologica Anton Dohrn, Naples, Italy

Read the full research article online: A king and vassals’ tale: Molecular signatures of clonal integration in Posidonia oceanica under chronic light shortage

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