agronomy Article First Steps to Domesticate Hairy Stork’s-Bill (Erodium crassifolium) as a Commercial Pharmaceutical Crop for Arid Regions Ofer Guy 1,*, Shabtai Cohen 1, Hinanit Koltai 2 , Moran Mazuz 2, Moran Segoli 1 and Amnon Bustan 1 1 Ramat Negev Desert Agro-Research Center (RNDARC), Ramat Negev Works Ltd., D.N. Halutza 8551500, Israel; [email protected] (S.C.); [email protected] (M.S.); [email protected] (A.B.) 2 Department of Ornamental Horticulture and Biotechnology, Institute of Plant Sciences, Agricultural Research Organization, Rishon LeZion 7528809, Israel; [email protected] (H.K.); [email protected] (M.M.) * Correspondence: [email protected]; Tel.: +972-50-3699001 Abstract: Hairy stork’s-bill (Erodium crassifolium) (HSB) is one of the few Geraniaceae species that produce tubers. While HSB tubers were occasionally used as a food source by desert nomads, they have not yet been taken up in the modern kitchen. Recently, HSB tubers were recognized as harboring potential to become an industrial pharmaceutical crop. The objective of this study was to determine a set of agricultural practices that would maximize the yield of the bioactive compounds of the present HSB genetic material. A generous and consistent irrigation regime of about 700 mm season−1 increased tuber yield and size. The optimal plant density on sandy soils was 16–20 plants m−2. Mineral nutrition, applied through fertigation, increased tuber yield from 0.6 to almost 1 kg m−2. Source-sink manipulations (consistent pruning of the reproductive organs) almost doubled the tuber yield. During 10 years of research, the adopted agricultural practices Citation: Guy, O.; Cohen, S.; Koltai, increased yield by an order of magnitude (from about 0.2–2.0 kg m−2) without any dilution of the H.; Mazuz, M.; Segoli, M.; Bustan, A. First Steps to Domesticate Hairy bioactive compounds. Nevertheless, further research and development are required to achieve HSB Stork’s-Bill (Erodium crassifolium) as a potential as an industrial field crop, including selection and breeding of outstanding infertile clones, Commercial Pharmaceutical Crop for optimization of fertigation, and development of various concrete pharmaceutical products. Arid Regions. Agronomy 2021, 11, 1715. https://doi.org/10.3390/ Keywords: arid land; Erodium crassifolium; medicinal crops; mineral nutrition; source-sink relations; agronomy11091715 underutilized species; plant domestication Academic Editor: Betty Benrey Received: 5 July 2021 1. Introduction Accepted: 26 August 2021 Hairy stork’s bill (HSB) (Erodium crassifolium L0Hér) is a Saharo-Arabian perennial Published: 27 August 2021 hemicryptophyte (i.e., buds are at or near the soil surface) common in shrub-steppes of arid southeast Mediterranean regions. The species is distributed from northwest at Crete [1], Publisher’s Note: MDPI stays neutral through few Aegean Sea islands [2], the Libyan [3] and Egyptian coasts [4,5], north Sinai with regard to jurisdictional claims in Peninsula [4,6], Cyprus [7], the Negev Desert of Israel [8], until Edom mountains of Jordan published maps and institutional affil- iations. and Saudi-Arabia deserts, on southeast [9]. In Israel, HSB is found in the Negev and Judean deserts, where the annual rainfall is in the range of 30–250 mm. The species is most abundant in the stony and arid loess soils and on the slopes of limestone hills [8]. There are several accessions of HSB ecotypes in the Israeli plant gene bank at the Agricultural Research Organization (ARO), however, differences between ecotypes have not been Copyright: © 2021 by the authors. characterized. The life cycle of HSB is described in Table1. Germination begins after the Licensee MDPI, Basel, Switzerland. first effective rain event, and an early vegetative phase occurs, forming typical rosette leaves. This article is an open access article During spring, further vegetative and reproductive growth waves occur, the intensity and distributed under the terms and conditions of the Creative Commons size of which depend on water availability [10]. Hairy stork’s bill is among the few plants Attribution (CC BY) license (https:// of the Geraniaceae family to produce tubers. The first tubers occur soon after germination creativecommons.org/licenses/by/ and thereafter, during the vegetative phase. The tubers are located on roots at a depth of 4.0/). 5–20 cm and are typically small and spherical (1–2 cm in diameter). Bedouin ethnobotanical Agronomy 2021, 11, 1715. https://doi.org/10.3390/agronomy11091715 https://www.mdpi.com/journal/agronomy Agronomy 2021, 11, x FOR PEER REVIEW 2 of 14 Agronomy 2021, 11, 1715 2 of 13 after germination and thereafter, during the vegetative phase. The tubers are located on roots at a depth of 5–20 cm and are typically small and spherical (1–2 cm in diameter). wisdomBedouin holds ethnobotanical that the tubers wisdom are edibleholds andthat asthe such tubers local are Bedouin edible and tribes as are such their local primary Bed- usersouin tribes [8]. HSB are tuberstheir primary have a users light sweet[8]. HSB taste, tubers and have their a bestlight qualitysweet taste, is in and late their winter best or earlyquality spring, is in late when winter they or are early whitish spring, in color when [8 they]. are whitish in color [8]. TableTable 1. 1.Life Life cycle cycle and and phenological phenological developmentdevelopment ofof HSBHSB asas observedobserved inin our irrigated fields.fields. Month December January February March April May June Week of Year 51 52 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Imbibition Developmental Germination stages Vegetative Tubers production Bloom Fruiting + seed dispersal Irrigation 6 mm day−1 4 mm day−1 (mm month−1) 84 152 120 124 120 80 While their culinary appeal is somewhat dull, recent studies in our labs have demonstratedWhile their that culinary HSB tubers appeal harbor is somewhat significant dull, pharmaceutical recent studies in potential our labs [10,11]. have demon- Elec- stratedtrochemical that HSB analysis tubers of harborthe water-soluble significant pharmaceuticalextract from HSB potential tubers [revealed10,11]. Electrochem- significant icalreducing analysis power of the and water-soluble identified at extractleast six from groups HSB of tubersantioxidants revealed (data significant not shown). reducing Frac- powertionation and of identified the tubers at′ ethanolic least six groupsextract of(EE) antioxidants and subsequent (data in-vitro not shown). evaluations Fractionation of pos- 0 ofsible the anti-inflammatory tubers ethanolicextract capacities (EE) revealed and subsequent significantin-vitro activityevaluations in fractions of F3 possible and F4, anti- as inflammatorywell as in the capacities original EE revealed and the significant pooled fractions, activity in PF fractions [10,11]. F3 Biochemical and F4, as wellanalyses as in theshowed original that EE F4 and comprised the pooled mainly fractions, epigalloca PF [10techin,,11]. Biochemical trans- and analysescis-catechin, showed and thatgallic F4 comprisedacid, all of mainly which epigallocatechin, are known for trans- their and robust cis-catechin, bioactive and capacities, gallic acid, allincluding of which an- are knownti-inflammatory for their robustactivity bioactive [12–18]. capacities, Interestingl includingy, the bioactivity anti-inflammatory of F4 was activity significantly [12–18]. Interestingly,greater than that the bioactivityof each compound of F4 was alone significantly at its corresponding greater than concentration that of each compound [11] indi- alonecating at synergic its corresponding relationships concentration in the natural [11 ex]tract. indicating Furthermore, synergic recently relationships we have in theshown nat- 0 uralthat extract.HSB tubers Furthermore,′ extracts recentlydisplayed we significantly have shown stronger that HSB anti-inflammatory tubers extracts displayed capacity significantlycompared to stronger extracts anti-inflammatory of green tea (Camellia capacity sinensis compared) and turmeric to extracts (Curcuma of green longa tea ()Camel- [11], liawell-known sinensis) and sources turmeric of anti-oxidative (Curcuma longa and)[ bioactive11], well-known compounds sources [12,19]. of anti-oxidative and bioactiveAn essential compounds demand [12,19 for]. the domestication of a given plant species must begin with a recognitionAn essential of significant demand for potential the domestication benefits that of it a may given provide. plant species Later steps must include, begin with and a recognitionnot necessarily of significant in the following potential order, benefits selection that it mayfor outstanding provide. 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