International Journal of Molecular Sciences Review Seed Germination in Oil Palm (Elaeis guineensis Jacq.): A Review of Metabolic Pathways and Control Mechanisms Jing Cui 1, Emmanuelle Lamade 2,3 and Guillaume Tcherkez 1,4,* 1 Research School of Biology, ANU Joint College of Science, Australian National University, Canberra, 2601 ACT, Australia; [email protected] 2 CIRAD, UPR Systèmes de Pérennes, 34398 Montpellier, France; [email protected] 3 Systèmes de Pérennes, Université de Montpellier, CIRAD, 34398 Montpellier, France 4 Institut de Recherche en Horticulture et Semences (IRHS), Université d’Angers, INRAE Angers, 42 rue Georges Morel, 49782 Beaucouzé cedex, France * Correspondence: [email protected] Received: 1 June 2020; Accepted: 12 June 2020; Published: 13 June 2020 Abstract: Oil palm is an oil-producing crop of major importance at the global scale. Oil palm mesocarp lipids are used for myriads industrial applications, and market demand has been growing for decades. In addition, oil palm seeds are oleaginous, and the oil extracted therefrom can be used for several purposes, from food to cosmetics. As such, there is a huge need in oil palm seeds to maintain the global cohort of more than 2 billion trees. However, oil palm seed germination is a rather difficult process, not only to break dormancy, but also because it is long and often reaches lower-than-expected germination rates. Surprisingly, despite the crucial importance of germination for oil palm plantation management, our knowledge is still rather limited, in particular about germinating oil palm seed metabolism. The present review incorporates different pieces of information that have been obtained in the past few years, in oil palm and in other palm species, in order to provide an overview of germination metabolism and its control. Further insights can also be gained from other oleaginous model plants, such as Arabidopsis or canola, however, palm seeds have peculiarities that must be accounted for, to gain a better understanding of germinating seed metabolism. Keywords: oil palm; seed; lipid remobilization; germination; metabolism; haustorium 1. Introduction Oil palm (Elaeis guineensis Jacq.) is presently the most productive oil crop, with a total global cultivation area of 19 million ha, and a recorded production of 0.27 gigatons of fruits and 71.4 megatons of palm oil [1]. This huge cultivated surface area represents about 2.7 billion trees. On average, oil palm 1 fields are generally renewed every 25 y, thus having an average replanting turn-over of 4% y− [2], meaning that each year, about 100 million trees have to be replaced. In addition to the increase in cultivated surface area in the past decades, this generates a huge demand in oil palm sapling cultivation in nurseries and, of course, in seedling production from seed germination or in vitro cloning (Figure1) (for a review on oil palm seed distribution and management, see [ 3]). Developing new crosses or hybrids (e.g., E. guineensis x oleifera) associated with better resistance to diseases (such as fatal yellowing) also requires growing palms from seeds. However, seed germination is still a hurdle in oil palm cultivation—as in many palm species—because of the relatively short seed storage time (preferably less than 16 weeks), methods required to break dormancy, and long germination and seedling establishment time, up to 9 months in nursery and up to several years in nature. Int. J. Mol. Sci. 2020, 21, 4227; doi:10.3390/ijms21124227 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 13 Int.dormancy, J. Mol. Sci. 2020 and, 21 long, 4227 germination and seedling establishment time, up to 9 months in nursery 2and of 13 up to several years in nature. 250 200 trees) 6 150 100 Global replanting (10 replanting Global 50 0 1970 1980 1990 2000 2010 2020 Year FigureFigure 1. 1.Estimated Estimated global global demand demand in in oil oil palm palm seedlings seedlings for for new new plantations plantations and and turn-over turn-over of of old old plantations.plantations. Computed Computed from from total total world world oil oil palm palm cultivation cultivation surface surface areaarea usingusing anan average density of −11 of143 trees ha− (FAO(FAO 2018). 2018). The The arrow arrow shows shows the the year year 2015 where totaltotal cultivatedcultivated areaarea reachedreached a a maximum.maximum. Surprisingly,Surprisingly, despite despite these these di difficultiesfficulties to to germinate germinate andand the high demand demand at at the the global global scale, scale, the thephysiology physiology of ofoil oilpalm palm germination germination and and seedling seedling establishment establishment is not is notvery very well well known. known. Most Mostmetabolic metabolic studies studies were were carried carried out outin the in the1980s 1980s [4–7] [4 –and,7] and, since since then, then, there there has hasbeen been very very little littleprogress progress in inour our knowledge knowledge of of molecular molecular actors actors and metabolicmetabolic regulationsregulations involved involved in in germination germination strictostricto sensu, sensu, seed seed storage storage remobilization remobilization and seedling and seedling development development of oil palm. of Thisoil palm. species This produces species oilyproduces (oleaginous) oily (oleaginous) seeds encapsulated seeds encapsulated into a hard endocarp into a hard layer, endocarp forming alayer, kernel forming (photographs a kernel in(photographs Figure2). As in such, Figure oil palm2). As seeds such, areoil palm also usedseeds as are a sourcealso used of oilas a (palmist source of oil), oil with(palmist industrial oil), with applicationsindustrial applications that differ from that mesocarpdiffer from oil. mesocarp The prevalence oil. The prevalence of lipids in of kernels lipids alsoin kernels implies also specific implies metabolicspecific pathwaysmetabolic ofpathways remobilization, of remobilization, that is, lipid that degradation is, lipid degradation and conversion and toconversion sugars. In to this sugars. brief In review,this brief we willreview, summarize we will metabolic summarize aspects metabolic of oil palmaspects seed of germinationoil palm seed (lato germination sensu) using (lato recent sensu) datausing obtained recent not data only obtained in oil palm not only but alsoin oil in palm other bu closelyt alsorelated in other palm closely species related of the palm same species botanical of the tribesame (Cocoeae botanical). The tribe importance (Cocoeae of). The primary importance metabolism of primary in defining metabolism seed quality in defining has been seed summarized quality has recentlybeen summarized [8]. We thus recently take advantage [8]. We thus of the take present advant reviewage of tothe emphasize present review metabolic to emphasize aspects thatmetabolic are currentlyaspects unknownthat are currently and deserve unknown further and research, deserve infurt particular,her research, to find in particular, new avenues to find to optimize new avenues oil palmto optimize seed germination. oil palm seed germination. Int. J. Mol. Sci. 2020, 21, 4227 3 of 13 Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 3 of 13 FigureFigure 2. 2.Photographs Photographs of of germinated germinated oiloil palmpalm seeds:seeds: over overviewview of of seeds seeds as as they they are are in in nurseries nurseries upon upon delivery,delivery, in polyethylenein polyethylene bag bag (a); (a anatomy); anatomy of aof germinated a germinated seed seed (b), (b showing), showing one one the the germinative germinative pore (gpf),pore the (gpf), cotyledonary the cotyledonary petiole petiole (cp), cotyledonary (cp), cotyledo ligulenary ligule (cl), the(cl), radiclethe radicle (ra) and(ra) and the plumulethe plumule (plu). Photographed(plu). Photographed seeds are seeds at stageare atIV stage (see IV Figure (see Figure3 for the3 for definition the defini oftion stages). of stages). Photographs: Photographs:© ©the the author (Jing Cui). author (Jing Cui). 2. Setting2. Setting the the Scene: Scene: Specific Specific Germination Germination StagesStages ByBy definition, definition, germination germination is is the the processprocess byby which seeds break break their their quiescent quiescent life, life, imbibe imbibe and and startstart development development so so that that the the radicle radicle pierces pierces seedseed envelopesenvelopes (integuments and and endocarp). endocarp). In Inpalm palm treetree species, species, such such as as oil oil palm,palm, this definition definition has has to to be be modified, modified, to take to take into intoaccount account the fact the that fact the that thefirst first anatomical anatomical structure structure that that pier piercesces seed seed envelopes envelopes is not is the not radicle, the radicle, but a butspecific a specific structure structure that represents the cotyledonary petiole. In other words, radicle development (as well as plumule that represents the cotyledonary petiole. In other words, radicle development (as well as plumule development) are part of post-germinative events. The cotyledonary petiole is associated with (and development) are part of post-germinative events. The cotyledonary petiole is associated with attached to) the cotyledon (equivalent to the scutellum in grasses), which here forms a haustorium (and attached to) the cotyledon (equivalent to the scutellum in grasses), which here forms a haustorium (Figure 2; Figure 3). The haustorium