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Genetic Improvement of Arundo Donax L.: Opportunities and Challenges

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Genetic Improvement of Arundo Donax L.: Opportunities and Challenges plants Review Genetic Improvement of Arundo donax L.: Opportunities and Challenges Tommaso Danelli 1,2, Marina Laura 3, Marco Savona 3 , Michela Landoni 4, Fabrizio Adani 1,2 and Roberto Pilu 1,2,* 1 Gruppo Ricicla Labs—Department of Agricultural and Environmental Sciences—Production, Landscape and Agroenergy, Università’ Degli Studi di Milano, Via Celoria 2, 20133 Milan, Italy; [email protected] (T.D.); [email protected] (F.A.) 2 Agricultural Genetics Group—Department of Agricultural and Environmental Sciences—Production, Landscape and Agroenergy, Università’ Degli Studi di Milano, Via Celoria 2, 20133 Milan, Italy 3 CREA, Research Centre for Vegetable and Ornamental Crops, Corso Degli Inglesi 508, 18038 Sanremo, Italy; [email protected] (M.L.); [email protected] (M.S.) 4 Department of Biosciences, Università’ Degli Studi di Milano, Via Celoria 26, 20133 Milan, Italy; [email protected] * Correspondence: [email protected] Received: 10 October 2020; Accepted: 13 November 2020; Published: 16 November 2020 Abstract: Arundo donax L., the giant reed—being a long-duration, low-cost, non-food energy crop able to grow in marginal lands—has emerged as a potential alternative to produce biomass for both energy production, with low carbon emissions, and industrial bioproducts. In recent years, pioneering efforts have been made to genetically improve this very promising energy crop. This review analyses the recent advances and challenges encountered in using clonal selection, mutagenesis/somaclonal variation and transgenesis/genome editing. Attempts to improve crop yield, in vitro propagation efficiency, salt and heavy metal tolerance by clonal selection were carried out, although limited by the species’ low genetic diversity and availability of mutants. Mutagenesis and somaclonal variation have also been attempted on this species; however, since Arundo donax is polyploid, it is very difficult to induce and select promising mutations. In more recent years, genomics and transcriptomics data are becoming available in Arundo, closing the gap to make possible the genetic manipulation of this energy crop in the near future. The challenge will regard the functional characterization of the genes/sequences generated by genomic sequencing and transcriptomic analysis in a complex polyploid genome. Keywords: Arundo donax; clonal selection; somaclonal variation; in vitro culture; genetic improvement 1. Introduction A. donax L. is a widespread species of unclear origin. This perennial grass grows spontaneously in temperate and tropical zones almost all over the world [1,2]. It can be found in ecosystems highly altered by anthropic activity and along riparian zones [3], where it often acts as an invasive weed reducing biodiversity [4], and brings an increased risk of wildfires and floods [5]. The roots can grow to 5 m in depth [1,6] and canes can reach 8–10 m in height and 3–4 cm in diameter (Figure1). The leaves are flat, 5–8 cm wide and 30–100 cm long, inserted alternately in two ranks [1,7,8]. In southern Europe, new canes sprout continuously from rhizomes, starting in early March until August to November, when flowering takes place. Senescence follows in winter, with canes becoming yellow and generally losing leaves and inflorescences. Inflorescences are large plume-like panicles 30–100 cm long [7] that do not produce viable seeds [9–13]. Plants 2020, 9, 1584; doi:10.3390/plants9111584 www.mdpi.com/journal/plants Plants 2020, 9, x FOR PEER REVIEW 2 of 18 Plantsand generally2020, 9, 1584 losing leaves and inflorescences. Inflorescences are large plume-like panicles 30–1002 of 18 cm long [7] that do not produce viable seeds [9–13]. Figure 1. Crop field field of A. donax L. for energy purposes in thethe third year of cultivation. Studies ononA. A. donax donaxL. L. sterility sterility are are often often contradictory. contradictory. In fact,In fa thisct, this topic topic has yethas to yet be to clarified, be clarified, since asince drastic a drastic founder founder effect could effect explain could this,explain rather this, than rather it being than a consequenceit being a consequence of defective chromosomeof defective pairingchromosome in aneuploid pairing inA. aneuploid donax and A.A. donax micrantha and A.Lam. micrantha [14]. AtLam. first [14]. glance, At first in A.glance, donax in, maleA. donax and, femalemale and gametogenesis female gametogenesis fails right afterfails meiosis.right after Following meiosis. the Following megaspores’ the megaspores’ mother cell formationmother cell at theformation tetrad stage,at the three tetrad chalazal stage, megaspores three chalazal degenerate, megaspores while onedegenerate, micropilar while megaspore one micropilar enlarges, developsmegaspore a largeenlarges, nucleolus develops but noa embryolarge nucleolus sac, with thebut consequentno embryo proliferation sac, with ofthe dysfunctional consequent cellsproliferation and the of failure dysfunctional of ovule development.cells and the failur Pollene of grains’ ovule cell development. walls usually Pollen collapse grains’ by cell autolysis, walls withusually the collapse appearance by ofautolysis, large numbers with the of vacuolesappearance and of variable large numbers numbers of nucleivacuoles and and micronuclei. variable Despitenumbers this of nuclei being theand common micronuclei. result, Despite the formation this being of the a few common viable pollenresult, grainsthe formation is reported of a withfew aviable frequency pollen of grains 6.2% is [14 reported,15]. Meiosis with occursa frequency in less of than 6.2% 10% [14,15]. of microsporocytes, Meiosis occurs in and less no than formation 10% of ofmicrosporocytes, exine occurs in and the no microsporangium formation of exine [11 ].occursA. donax in thesterility microsporangium has been reported [11]. A. to donax be related sterility to alterationshas been reported in gametogenesis to be related and to fertilization alterations andin gametogenesis post-fertilization and development fertilization [and16]. post-fertilizationA. donax sterility mostdevelopment likely has [16]. various A. donax causes sterility that havemost led likely to its has agamic various propagation causes that strategy. have led Reproduction to its agamic is exclusivelypropagation asexual strategy. and occursReproduction through vegetativeis exclusively propagation asexual [17 and,18] byoccurs fragmentation through ofvegetative rhizomes andpropagation cane fragments, [17,18] whichby fragmentation are dispersed of by rhizomes floods or and by humancane fragments, activity [1 ,19which]. are dispersed by floodsThe or worldwideby human activity spread of [1,19].A. donax is related to several domestic and agricultural purposes such as the makingThe worldwide of walking-sticks, spread of baskets, A. donax mats, is related fishing to rods, several fences, domestic plant and stakes agricultural and musical purposes instruments’ such parts,as the especiallymaking of the walking-sticks, reeds for clarinets baskets, and mats saxophones, fishing [ 1rods,,8,20, 21fences,]. A. donaxplant isstakes supposed and musical to have spreadinstruments’ from Asia,parts,its especially native center, the reeds to America, for clarinets passing and saxo throughphones the [1,8,20,21]. Mediterranean A. donax area is [supposed15,22–25]. Otherto have authors spread suggest from Asia, that thisits na planttive originatedcenter, to America, in Mediterranean passing through regions fromthe Mediterranean native species area [26]. At[15,22–25]. least four Other other authors species suggest from the thatArundo this taxonplant areoriginated present in in Mediterranean the Mediterranean regions area: fromA. plinii nativeL., A.species collina [26].Ten., AtA. least mediterranea, four other andspeciesA. micranthafrom the ArundoLam. [27 taxon,28]. are Six present lineages in of theA. Mediterranean donax are supposed area: toA. beplinii distributed L., A. collina from Ten., Asia A. to mediterranea, the Mediterranean and A. basin,micrantha with Lam. a putative [27,28]. area Six oflineages origin of in theA. donax Western are andsupposed Southern to be edges distributed of theQinghai-Tibet from Asia to the Plateau Mediterr [29].anean The phylogenesis basin, with a of putativeA. donax areais still of origin debated, in asthe the Western hypothesis and Southern that this speciesedges of is the polyploid Qingha ori-Tibet allopolyploid Plateau [29]. is shared The phylogenesis by variousauthors of A. donax based is onstill its debated, macroscopic as the traits, hypoth suchesis as that the greatthis species vegetative is polyploid vigor and or the allopolyploid absence of fertile is shared seeds by [12 various,13,30]. Theauthors literature based dataon its about macroscopic the chromosome traits, such number as the ofgreatA. donax vegetativeL. show vigor some and discrepancies, the absence of from fertile an often-reportedseeds [12,13,30]. number The literature of 108–110 data chromosomes about the [12 chromosome,30–33], to 84 chromosomesnumber of A. [ 13donax], or seed-producingL. show some cytotypesdiscrepancies, with 72from chromosomes, an often-reported although thisnumber last result of was108–110 published chromosomes before the revised[12,30–33], classification to 84 ofchromosomes the genus Arundo [13], or[28 seed-producing]. cytotypes with 72 chromosomes, although this last result was publishedLarge-scale before cultivation the revised of classificationA. donax was of established the genus Arundo between [28]. the 1930s and the 1960s in
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