Emblematic Vachellia spp. naturally exposed to hyper-arid conditions, intensive grazing, and parasitism maintain a high nitrogen content and functional mutualistic nitrogen-fixing symbioses. AlUla region in Saudi Arabia has a rich history regarding mankind, local wildlife, and fertility islands suitable for leguminous species, such as the emblematic Vachellia spp. desert trees. In this region, we investigated the characteristics of desert legumes in two nature reserves (Sharaan and Madakhil), at one archaeological site (Hegra), and in open public domains et al. Ward and Jabal Abu Oud. Biological nitrogen fixation (BNF), isotopes, and N and C contents were investigated through multiple lenses, including parasitism, plant tissues, species identification, plant maturity, health status, and plant growth. The average BNF rates of 19 Vachellia gerrardii and 21 Vachellia tortilis trees were respectively 39 and 67%, with low signs of inner N content fluctuations (2.10-2.63% N) compared to other co-occurring plants. The BNF of 23 R. raetam was just as high, with an average of 65% and steady inner N contents of 2.25 ± 0.30%. Regarding parasitism, infected Vachellia trees were unfazed compared to uninfected trees, thereby challenging the commonly accepted detrimental role of parasites. Overall, these results suggest that Vachellia trees and R. raetam shrubs exploit BNF in hyper-arid environments to maintain a high N content when exposed to parasitism and grazing. These findings underline the pivotal role of plant-bacteria mutualistic symbioses in desert environments. All ecological traits and relationships mentioned are further arguments in favor of these legumes serving as keystone species for ecological restoration and agro-silvo-pastoralism in the AlUla region.

CIRAD UMR113 LSTM TA A 82⁄J Campus International de Baillarguet 34398 Montpellier Cedex 5 France

Department of Mycorrhizal Symbioses Institute of Botany Czech Academy of Sciences Lesní 322 Průhonice Czech Republic

Department of Plant Taxonomy and Nature Conservation University of Gdańsk Wita Stwosza 59 80 308 Gdańsk Poland

Department of Research and Development VALORHIZ 1900 Boulevard de la Lironde PSIII Parc Scientifique Agropolis 34980 Montferrier sur Lez France

Eco and Sols IRD Université de Montpellier CIRAD INRAE Institut Agro Montpellier France

Institut Systématique Evolution Biodiversité CNRS Sorbonne Université EPHE 57 rue Cuvier CP39 75005 Paris France

Institut Universitaire de France Paris France

Understanding Evolution Group Naturalis Biodiversity Center Darwinweg 2 2333 CR Leiden The Netherlands

Erratum In

Planta. 2024 May 15;259(6):154. doi: 10.1007/s00425-024-04436-9. PubMed

See more in PubMed

Abdel-Hamid AME, Elenazy HH, Abdel-Hameed UK. DNA barcoding of some taxa of genus Acacia and their phylogenetic relationship. Life. 2021;14:588–598. doi: 10.1080/26895293.2021.1938702. DOI

Aleid SM, Al-Khayri JM, Al-Bahrany AM. Date palm status and perspective in Saudi Arabia. In: Al-Khayri JM, Jain SM, Johnson DV, editors. Date palm genetic resources and utilization. Dordrecht: Springer; 2015. pp. 49–95.

Almazroui M. Simulation of present and future climate of Saudi Arabia using a regional climate model (PRECIS) Int J Climatol. 2013;33:2247–2259. doi: 10.1002/joc.3721. DOI

Almazroui M, Islam MN, Dambul R, Jones PD. Trends of temperature extremes in Saudi Arabia. Int J Climatol. 2014;34:808–826. doi: 10.1002/joc.3722. DOI

Al-Rowaily SL, El-Bana MI, Al-Bakre DA, et al. Effects of open grazing and livestock exclusion on floristic composition and diversity in natural ecosystem of Western Saudi Arabia. Saudi J Biol Sci. 2015;22:430–437. doi: 10.1016/j.sjbs.2015.04.012. PubMed DOI PMC

Al-Sharari N, Bakhashwain A, Elfeel A. Profiling and importance of underutilized neglected species of hyper arid climate of Saudi Arabia (Retama raetam—Retem): a review. Life Sci J. 2020;17:35–42. doi: 10.7537/marslsj170720.06. DOI

Al-Subhi AM, Al-Sadi AM, Al-Yahyai RA, et al. Witches’ broom disease of lime contributes to phytoplasma epidemics and attracts insect vectors. Plant Dis. 2021;105:2637–2648. doi: 10.1094/PDIS-10-20-2112-RE. PubMed DOI

Ansari AA, Siddiqui ZH, Alatawi FA, et al (2022) An Assessment of Biodiversity in Tabuk Region of Saudi Arabia: A Comprehensive Review. Sustainability 14:10564. 10.3390/su141710564

Barakat NAM, Laudadio V, Cazzato E, Tufarelli V. Potential contribution of Retama raetam (Forssk.) Webb & Berthel as a forage shrub in Sinai. Egypt Arid Land Res Manag. 2013;27:257–271. doi: 10.1080/15324982.2012.756561. DOI

Bchir A, Escalona JM, Gallé A, et al. Carbon isotope discrimination (δ13C) as an indicator of vine water status and water use efficiency (WUE): looking for the most representative sample and sampling time. Agric Water Manag. 2016;167:11–20. doi: 10.1016/j.agwat.2015.12.018. DOI

Bellakhdar J (1997) Contribution à l’étude de la pharmacopée traditionnelle au Maroc : la situation actuelle, les produits, les sources du savoir (enquête ethnopharmacologique de terrain réalisée de 1969 à 1992). Doctoral Thesis, Metz

Belsky AJ. Influences of trees on savanna productivity: tests of shade, nutrients, and tree-grass competition. Ecology. 1994;75:922–932. doi: 10.2307/1939416. DOI

Blakesley D, Allen A, Pellny TK, Roberts AV. Natural and induced polyploidy in Acacia dealbata Link. and Acacia mangium Willd. Ann Bot. 2002;90:391–398. doi: 10.1093/aob/mcf202. PubMed DOI PMC

Bowie M, Ward D. Water and nutrient status of the mistletoe Plicosepalus acaciae parasitic on isolated Negev Desert populations of Acacia raddiana differing in level of mortality. J Arid Environ. 2004;56:487–508. doi: 10.1016/S0140-1963(03)00067-3. DOI

Chowdhury S, Al-Zahrani M. Characterizing water resources and trends of sector wise water consumptions in Saudi Arabia. J King Saud Univ Eng Sci. 2015;27:68–82. doi: 10.1016/j.jksues.2013.02.002. DOI

Csárdi G, Nepusz T, Traag V, Horvát S, Zanini F, Noom D, Müller K (2024) igraph: Network Analysis and Visualization in R. R package version 1.6.0. 10.5281/zenodo.10369053

Do FC, Rocheteau A, Diagne AL, et al. Stable annual pattern of water use by Acacia tortilis in Sahelian Africa. Tree Physiol. 2008;28:95–104. doi: 10.1093/treephys/28.1.95. PubMed DOI

Ehleringer JR, Cook CS, Tieszen LL. Comparative water use and nitrogen relationships in a mistletoe and its host. Oecologia. 1986;68:279–284. doi: 10.1007/BF00384800. PubMed DOI

Green AK, Ward D, Griffiths ME. Directed dispersal of mistletoe (Plicosepalus acaciae) by Yellow-vented Bulbuls (Pycnonotus xanthopygos) J Ornithol. 2009;150:167–173. doi: 10.1007/s10336-008-0331-9. DOI

Hasanean H, Almazroui M. Rainfall: features and variations over Saudi Arabia, a review. Climate. 2015;3:578–626. doi: 10.3390/cli3030578. DOI

Hobbs JJ, Krzywinski K, Andersen GL, et al. Acacia trees on the cultural landscapes of the Red Sea Hills. Biodivers Conserv. 2014;23:2923–2943. doi: 10.1007/s10531-014-0755-x. DOI

Ismail M, Ahmad A, Nadeem M, et al. Development of DNA barcodes for selected Acacia species by using rbcL and matK DNA markers. Saudi J Biol Sci. 2020;27:3735–3742. doi: 10.1016/j.sjbs.2020.08.020. PubMed DOI PMC

Kassambara A, Mundt F (2020) factoextra: Extract and visualize the results of multivariate data analyses. R Package Version 1.0.7

Küppers M, Küppers BIL, Neales TF, Swan AG. Leaf gas exchange characteristics, daily carbon and water balances of the host/mistletoe pair Eucalyptus behriana F. Muell. and Amyema miquelii (Lehm. ex Miq.) Tiegh. at permanently low plant water status in the field. Trees. 1992;7:1–7. doi: 10.1007/BF00225225. DOI

Kyalangalilwa B, Boatwright JS, Daru BH, et al. Phylogenetic position and revised classification of Acacia s.l. (Fabaceae: Mimosoideae) in Africa, including new combinations in Vachellia and Senegalia. Bot J Linn Soc. 2013;172:500–523. doi: 10.1111/boj.12047. DOI

Lahaye R, van der Bank M, Bogarin D, et al. DNA barcoding the floras of biodiversity hotspots. Proc Natl Acad Sci USA. 2008;105:2923–2928. doi: 10.1073/pnas.0709936105. PubMed DOI PMC

Lê S, Josse J, Husson F. FactoMineR: an R package for multivariate analysis. J Stat Softw. 2008;25:1–18. doi: 10.18637/jss.v025.i01. DOI

León-González AJ, Navarro I, Acero N, et al. Genus Retama: a review on traditional uses, phytochemistry, and pharmacological activities. Phytochem Rev. 2018;17:701–731. doi: 10.1007/s11101-018-9555-3. DOI

Mabberley DJ. Mabberley’s plant-book: a portable dictionary of plants, their classification and uses. 4. Cambridge: Cambridge University Press; 2017.

Meinhardt LW, Rincones J, Bailey BA, et al. Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao: What’s new from this old foe? Mol Plant Pathol. 2008;9:577–588. doi: 10.1111/j.1364-3703.2008.00496.x. PubMed DOI PMC

Munzbergova Z, Ward D. Acacia trees as keystone species in Negev desert ecosystems. J Veg Sci. 2002;13:227–236. doi: 10.1111/j.1654-1103.2002.tb02043.x. DOI

Ndoye I, Gueye M, Danso SKA, Dreyfus B. Nitrogen fixation in Faidherbia albida, Acacia raddiana, Acacia senegal and Acacia seyal estimated using the 15N isotope dilution technique. Plant Soil. 1995;172:175–180. doi: 10.1007/BF00011319. DOI

Odee DW, Wilson J, Omondi S, et al. Rangewide ploidy variation and evolution in Acacia senegal: a North-South divide? AoB Plants. 2015;7:plv011. doi: 10.1093/aobpla/plv011. PubMed DOI PMC

Osman AK, Al-Ghamdi F, Bawadekji A. Floristic diversity and vegetation analysis of Wadi Arar: a typical desert Wadi of the Northern Border region of Saudi Arabia. Saudi J Biol Sci. 2014;21:554–565. doi: 10.1016/j.sjbs.2014.02.001. PubMed DOI PMC

Panvini AD, Eickmeier WG. Nutrient and water relations of the mistletoe Phoradendron leucarpum (Viscaceae): How tightly are they integrated? Am J Bot. 1993;80:872–878. doi: 10.2307/2445506. DOI

Parker WJ, Oster J, Brassard LA (2005) US Patent No. 6,958,372. US Patent and Trademark Office, Washington, DC

Pires TL, Lange D, Del-Claro K. Witches’ brooms increases arthropod-plant interactions in Ouratea hexasperma (Baill.) (Ochnaceae) Acta Oecol. 2020;102:103508. doi: 10.1016/j.actao.2019.103508. DOI

R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

Rahman MA, Mossa JS, Al-Said MS, Al-Yahya MA. Medicinal plant diversity in the flora of Saudi Arabia 1: a report on seven plant families. Fitoterapia. 2004;75:149–161. doi: 10.1016/j.fitote.2003.12.012. PubMed DOI

Rao GP, Mitra S, Ayanur G, et al. Vachellia nilotica: a new host of ‘Candidatus phytoplasma asteris’ and ‘Ca. P. trifolii’-related strains in India. Phytopathogenic Mollicutes. 2021;11:64–68. doi: 10.5958/2249-4677.2021.00009.8. DOI

Russow R, Veste M, Littmann T. Using the natural 15N abundance to assess the main nitrogen inputs into the sand dune area of the North-Western Negev desert (Israel) Isotopes Environ Health Stud. 2004;40:57–67. doi: 10.1080/10256010310001646554. PubMed DOI

Schulze E-D, Turner NC, Glatzel G. Carbon, water and nutrient relations of two mistletoes and their hosts: a hypothesis. Plant Cell Environ. 1984;7:293–299. doi: 10.1111/1365-3040.ep11589756. DOI

Schulze E-D, Gebauer G, Ziegler H, Lange OL. Estimates of nitrogen fixation by trees on an aridity gradient in Namibia. Oecologia. 1991;88:451–455. doi: 10.1007/BF00317592. PubMed DOI

Seraphin P, Gonçalvès J, Hamelin B, et al. Influence of intensive agriculture and geological heterogeneity on the recharge of an arid aquifer system (Saq–Ram, Arabian Peninsula) inferred from GRACE data. Hydrol Earth Syst Sci. 2022;26:5757–5771. doi: 10.5194/hess-26-5757-2022. DOI

Shearer G, Kohl D. N2-Fixation in field settings: estimations based on natural 15N abundance. Funct Plant Biol. 1986;13:699. doi: 10.1071/PP9860699. DOI

Tonn B, Porath I, Lattanzi FA, Isselstein J. Urine effects on grass and legume nitrogen isotopic composition: pronounced short-term dynamics of δ15N. PLoS ONE. 2019;14:e0210623. doi: 10.1371/journal.pone.0210623. PubMed DOI PMC

Vasilyeva GV, Zhuk EA, Goroshkevich SN. Effect of witches’ broom mutation on growth of seedlings. Silvae Genet. 2020;69:123–129. doi: 10.2478/sg-2020-0017. DOI

Waly NM, Emad HM. Taxonomical studies of some Acacia spp. growing in Saudi Arabia. Bull Environ Pharmacol Life Sci. 2012;1:55–62.

Watling JR, Press MC. Impacts of infection by parasitic angiosperms on host photosynthesis. Plant Biol. 2001;3:244–250. doi: 10.1055/s-2001-15195. DOI

Wei T, Simko V, Levy M et al (2021) corrplot: Visualization of a correlation matrix. R Package Version 0.92

Winters G, Otieno D, Cohen S, et al. Tree growth and water-use in hyper-arid Acacia occurs during the hottest and driest season. Oecologia. 2018;188:695–705. doi: 10.1007/s00442-018-4250-z. PubMed DOI