Successes and challenges in the sustainable cultivation of edible mycorrhizal fungi - furthering the dream

Abstract

The cultivation of edible mycorrhizal fungi (EMF) has made great progress since the first cultivation of Tuber melanosporum in 1977 but remains in its infancy. Five cultivation steps are required: (1) mycorrhizal synthesis, (2) mycorrhiza development and acclimation, (3) out-planting of mycorrhizal seedlings, (4) onset of fructification, and (5) performing tree orchards. We provide examples of successes and challenges associated with each step, including fruiting of the prestigious chanterelles in Japan recently. We highlight the challenges in establishing performing tree orchards. We report on the monitoring of two orchards established between Lactarius deliciosus (saffron milk cap) and pines in New Zealand. Saffron milk caps yields reached 0.4 and 1100 kg/ha under Pinus radiata and P. sylvestris 6 and 9 y after planting, respectively. Canopy closure began under P. radiata 7 y after planting, followed by a drastic reduction of yields, while P. sylvestris yields still hovered at 690 to 780 kg/ha after 11 y, without canopy closure. The establishment of full-scale field trials to predict yields is crucial to making the cultivation of EMF a reality in tomorrow's cropping landscape. Sustainable EMF cultivation utilizing trees in non-forested land could contribute to carbon storage, while providing revenue and other ecosystem services.

Keywords: Lactarius deliciosus; ecosystem services; forest mushroom; orchard; truffle.

Fig. 1.. - Cultivation cycle of an edible mycorrhizal fungus. The five steps involved are illustrated based on the example of Lactarius deliciosus (saffron milk cap) cultivated in association with Pinus radiata (Monterey pine).

Fig. 2.. - Mother plant technique used to inoculate Pinus radiata seedlings with naturallyoccurring Boletus edulis (porcini). A:P. radiata seedlings growing underneath porcini-productive oak trees at the University of Canterbury, Christchurch, New Zealand (2007). Note the fruiting bodies of porcini (arrow) growing next to the pine seedlings. B: Ectomycorrhiza of B.edulis formed on an unearthed P. radiata seedling. Bar: 190 μm.

Fig. 3.. - Ectomycorrhizae and fruiting-bodies of commercial truffle species in New Zealand. A–C: Ectomycorrhizae of Tuber melanosporum × Quercus robur, T. aestivum × Q. ilex, and T. borchii × Pinus pinea formed by spore inoculation at Southern Woods Nursery, Templeton, New Zealand. D: Accidental presence of T. borchii mycorrhizae (arrowhead) co-occurring with T. aestivum ectomycorrhizae (arrows) on a T. aestivum-inoculated Q. robur seedling. E, F: High-value truffles cultivated in truffières in Canterbury, New Zealand: T. melanosporum with truffle dog Cassie (Tewnion Truffière, Old West Coast Road, Christchurch) and T. borchii (harvested from the trial orchard at the Lincoln Farm of The New Zealand Institute for Plant & Food Research Ltd, Lincoln),respectively. Bars: A 550 μm; B 440 μm; C 350 μm; D 580 μm.

Fig. 4.. - Layout of the Pinus radiata orchard (see also Guerin-Laguette et al., 2014, 2020) and historyof mushroom production for each tree. As of 2020, the orchard is composed of 39 trees over ≈ 1,000 m². Each F number locates a P. radiata tree. The graphs indicate the numbers of fruiting bodies harvested from each tree from 2010 to 2019, exceptfor trees F27, 25 and 16 where no mushroom number could be assigned to thesetrees in 2019. Abundant fructification (96 mushrooms) was found, mostly at the south of tree F27, spread in the grassy patch left by the disappearance ofnear by trees (F52, 16 and 22). This could correspond to underground Lactarius deliciosus mycelium being mycorrhizal with the root systems of nearby standing trees. This fructification was counted as coming from edge trees in 2019. Trees in orange are considered ‘inside’ in comparison with those in black that are on the edge of the orchard (see also (Fig. 9). A cross indicates a dead tree: Tree F52 died during the first year after planting while trees F22 and F16 were lost to wind storms in 2013 and 2014, respectively (vertical red bars mark the death).

Fig. 5.. - Layout of the Pinus sylvestris (Scots pine) orchard and history of mushroom production for each tree. The orchard is composed of 10 trees over 250 m². Each square indicates a P. sylvestris tree inoculated with a distinct Lactarius deliciosus isolate, i.e. D60, D68, D74 or D64 (see also Guerin-Laguette et al., 2020). The graphs indicate the numbers of fruiting bodies harvested from each tree from 2012 to 2019.

Fig. 6.. - Yields (kg/ha) of Lactarius deliciosus (saffron milk caps) produced by the Pinus radiata or P. sylvestris orchard over ten and eight production years, respectively. Orchards were established in Dec 2007.

Fig. 7.. - Views of the Pinus radiata and P. sylvestris orchards including grass cover or pine needle litteraround trees. A: View of the P. radiata orchard (west side) and its canopy closure on 19 Mar 2019; B: The needle deposition layer is apparent inside the P.radiata orchard on 11 May 2015; C: Comparative view on 22 Jan 2019 of the growth of trees of the saffron milk cap x P.sylvestris orchard (left) versus that of Boletus edulis x P. radiata trees (right), all planted in 2007; D: Thick needle litter inside the P. radiata orchard (from left, trees F23 and F60) with mushrooms growing underneath the litter around tree F60 on 15 May 2019; E: Partial view of the east side of the P. sylvestris orchard (from left, trees P4 and ⑯) on 22 Jan 2019 showing the lawn cover that can still develop around trees 11 y after plantation because of the lack of canopy closure.

Figure 8. Fruiting and harvests of saffron milk cap (Lactarius deliciosus) under two pine species. A–C: Morphological characteristics of L. deliciosus basidiomata. A: Concentric circles on the cap (Pinus radiata, 29 Jan 2018). B: Abundant milk coming off the stipe of freshly harvested fruiting-body (P. radiata, 2 Mar 2018). C: ‘Scrobicules’ or orange stains on the stipe (P.sylvestris, 30 Apr 2019). D–F: P. radiata site. D: Grass cover and mushroom production on the edge of the orchard, south of tree F59, 30 Apr 2019. E: Mushroom production inside the orchard under the pine needle litter close to the trunk, southwest of tree F60, 30 Apr 2019. F: One day-harvest under tree 60, 5 March 2018. G–I: P.sylvestris site. G: Harvest from several trees on 3 May 2019. H: High density of fructification around tree ⑧ (75 mushrooms harvested around that tree on 3 May 2019). I: Example of fructifications in the needle litter below the canopy of P. sylvestris, 3 May 2019.

Fig. 9.. - Evolution of the number of mushrooms produced by trees according to their position in the Pinus radiata orchard, i.e. ‘edge trees’ versus ‘inside trees’ (see Fig. 4), every year since the start of fruiting in 2010. Canopy closure and needle deposition started approximately in 2015.