Floral and Pollen Traits of Moringa Oleifera Lam. and Moringa Peregrina (Forssk.) Fiori Provide Reproductive Adaptations for Arid Conditions
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agronomy Article Floral and Pollen Traits of Moringa oleifera Lam. and Moringa peregrina (Forssk.) Fiori Provide Reproductive Adaptations for Arid Conditions Yiftach Vaknin 1,*, Dan Eisikowitch 2 and Adina Mishal 3 1 Department of Natural Resources, Institute of Plant Sciences, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O. Box 15159, Rishon LeZion 7505101, Israel 2 Department of Plant Sciences, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel; [email protected] 3 Faculty of Science, Kibbutzim College of Education, Tel Aviv University, 149 Derech Namir, Tel Aviv 6250769, Israel; [email protected] * Correspondence: [email protected]; Tel.: +972-3-968-3486 Abstract: Our study attempted to elucidate the significance of floral and pollen traits of the highly nutritious tropical trees Moringa oleifera and Moringa peregrina for their reproductive success under arid conditions. We found that the pollen grains of both species were immersed in a pollenkitt that constituted ~60% of the pollen. Successful pollination was achieved by large bees inserting the pollen into a narrow stylar tube. We found that, upon removal of the pollenkitt, approximately 65% fewer pollen grains penetrated the stylar tube for both species. The pollenkitt protected against heat and desiccation, while removing the pollenkitt resulted in significantly reduced levels of the viability Citation: Vaknin, Y.; Eisikowitch, D.; of pollen grains, especially in M. oleifera, and significantly reduced levels of germinability in both Mishal, A. Floral and Pollen Traits of species. The stylar tube provided high protection for pollen grains against heat and desiccation even Moringa oleifera Lam. and Moringa when the pollenkitt was removed. Chemical analysis of pollenkitts of the two species revealed a peregrina (Forssk.) Fiori Provide waxy blend of 21 hydrocarbon compounds, in which n-alkanes constituted >90% of the compounds Reproductive Adaptations for Arid and their identity corresponded to known plant and animal hydrocarbons, associated with protection Conditions. Agronomy 2021, 11, 1090. against heat and water stress. We concluded that, under arid conditions, the reproductive success of https://doi.org/10.3390/ both Moringa species is potentially enhanced by their unique floral and pollen traits. This supports agronomy11061090 the prospect of cultivating M. oleifera and Moringa peregrina as food crops in arid regions across the globe. Academic Editor: Yehoshua (Shuki) Saranga Keywords: arid conditions; pollen adhesion; pollen germinability; pollenkitt; pollen viability; reproductive adaptation; water stress Received: 11 May 2021 Accepted: 25 May 2021 Published: 27 May 2021 Publisher’s Note: MDPI stays neutral 1. Introduction with regard to jurisdictional claims in Moringaceae is a family consisting of 13 known perennial species from a dry tropical published maps and institutional affil- origin [1] and certain species, such as M. oleifera and M. peregrina, can potentially be grown iations. under arid conditions. Moringa oleifera, also known as “the miracle tree,” is the most widely distributed and economically important tree species in this family. Its leaves and immature pods are highly nutritious. It is traditionally utilized as a food crop throughout the dry tropics in Asia, Africa, and America, with very little cultivation in arid regions [2]. It is Copyright: © 2021 by the authors. also cultivated as a source of seed oil for food, bioenergy, and cosmetics [3–5]. Various Licensee MDPI, Basel, Switzerland. plant parts are used as natural medicine [6,7], and seed powder is used as a coagulant for This article is an open access article water purification [8]. Moringa peregrina is the second most utilized Moringa species [1]. distributed under the terms and It is a wild tree, highly tolerant to heat and drought [9], originating in the desert along conditions of the Creative Commons the Red Sea throughout the Arabian Peninsula. M. peregrina is a highly nutritious tree Attribution (CC BY) license (https:// grown primarily for human consumption, medicinal purposes, and animal fodder [10]. creativecommons.org/licenses/by/ The seeds of M. peregrina provided oil for food and cosmetics in antiquity [11]. However, 4.0/). Agronomy 2021, 11, 1090. https://doi.org/10.3390/agronomy11061090 https://www.mdpi.com/journal/agronomy Agronomy 2021, 11, x FOR PEER REVIEW 2 of 17 Agronomy 2021, 11, 1090 2 of 17 of M. peregrina provided oil for food and cosmetics in antiquity [11]. However, its com- mercial value as a food and medicinal and industrial commodity has rarely been explored its commercial value as a food and medicinal and industrial commodity has rarely been [12,13]. explored [12,13]. M. oleifera is cultivated in tropical climatic regions worldwide, while arid regions are M. oleifera is cultivated in tropical climatic regions worldwide, while arid regions are being carefully explored for its cultivation. M. peregrina, on the other hand, is well-adapted being carefully explored for its cultivation. M. peregrina, on the other hand, is well-adapted to arid conditions with <200–300 mm rainfall and is, therefore, considered to be drought- to arid conditions with <200–300 mm rainfall and is, therefore, considered to be drought- tolerant. Both Moringa species require hot and dry conditions with sufficient water supply tolerant. Both Moringa species require hot and dry conditions with sufficient water supply forfor growthgrowth andand reproduction.reproduction. WhenWhen growngrown inin aridarid regionsregions suchsuch asas thethe NegevNegev andand AravaArava DesertsDeserts inin Israel, Israel, they they have have better better performances, performances, both both vegetatively vegetatively and reproductively,and reproductively, than whenthan when grown grown under under wetter wetter and colder and colder conditions, conditions, as long as as long they as are they sufficiently are sufficiently irrigated ir- andrigated saturation and saturation of the soil of withthe soil water with is wa avoidedter is avoided by proper by drainage proper drainage [14]. [14]. InIn our previous previous study, study, we we assessed assessed both both M.M. oleifera oleifera andand M. peregrinaM. peregrina as potentialas potential seed- seed-oiloil and seed-protein and seed-protein sources sources under under semi-arid, semi-arid, Mediterranean Mediterranean conditions conditions [15]. We [15 ].found We foundthat M. that oleiferaM. oleifera was betterwas bettersuited suitedfor oil forand oil protein and protein production production than M. than peregrinaM. peregrina under undersemi-arid semi-arid conditions. conditions. It produced It produced more seeds more more seeds predictably more predictably than M. than peregrinaM. peregrina. M. per-. M.egrina peregrina, on the, on other the otherhand, hand, produced produced larger larger seeds seeds with withhigher higher oil concentrations oil concentrations and andwas wasless lesssusceptible susceptible to local to local diseases diseases than than M. oleiferaM. oleifera. TheThe floralfloral morphologicmorphologic andand chemicalchemical traitstraits andand thethe pollinationpollination servicesservices providedprovided byby pollenpollen vectorsvectors ofof M.M. oleiferaoleifera andand M.M. peregrinaperegrinaare arevital vitalto to their their reproductive reproductive success. success. BothBoth M.M. oleiferaoleifera andand M.M. peregrinaperegrinahave have zygomorphiczygomorphic andand horizontallyhorizontally orientedoriented hermaphroditichermaphroditic flowersflowers withwith fivefive sepals,sepals, fivefive petals,petals, andand fivefive unequalunequal stamensstamens surroundingsurrounding aa singlesingle pistilpistil (Figure(Figure1 1)) consisting consisting of of one one open-type open-type stigma stigma and and a a hollow hollow stylar stylar tube. tube. At At maturity, maturity, the the posteriorposterior petalpetal remainsremains erect,erect, whilewhile thethe othersothers areare reflexedreflexedtogether together withwiththe thesepals. sepals. TheThe intermediateintermediate andand frontfront petalspetals areare curvedcurved forward,forward, bearingbearing shortshort trichomestrichomes onon theirtheir ventralventral side,side, andand theythey function function as as a a landing landing platform platform for for visiting visiting insects insects [16 [16].]. Flower Flower anthesis anthesis of M. of oleiferaM. oleiferais associated is associated with with a temperature a temperature range range of 27–29 of 27–29◦C and °C relativeand relative humidity humidity of 68–78%. of 68– The78%. flowers The flowers are protandrous are protandrous and herkogamous. and herkogamous. At anthesis, At anthesis, the anthers the dehisceanthers through dehisce longitudinalthrough longitudinal slits releasing slits releasing spheroidal spheroidal pollen grainspollen (~35grainsµm) (~35 while µm) thewhile style the remainsstyle re- shortermains shorter than the than anthers the anthers [17]. After [17]. ~24After h, ~24 the h, style the style elongates elongates beyond beyond the length the length of the of anthers,the anthers, and and the stigmathe stigma becomes becomes receptive receptive for the for nextthe next 48 h 48 [18 h]. [18]. A similar A similar floral floral structure struc- andturephenological and phenological pattern pattern were were recorded recorded for M. for peregrina M. peregrinaby Vaknin by Vaknin and Mishal and Mishal [15]. [15]. FigureFigure 1.1. OpenOpen flowersflowers ofof M.M.