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Primordium Initiation Drives Tree Growth Ronald M Primordium initiation drives tree growth Ronald M. Lanner To cite this version: Ronald M. Lanner. Primordium initiation drives tree growth. Annals of Forest Science, Springer Nature (since 2011)/EDP Science (until 2010), 2017, 74 (1), pp.11. 10.1007/s13595-016-0612-z. hal- 01703449 HAL Id: hal-01703449 https://hal.archives-ouvertes.fr/hal-01703449 Submitted on 7 Feb 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Annals of Forest Science (2017) 74: 11 DOI 10.1007/s13595-016-0612-z ORIGINAL PAPER Primordium initiation drives tree growth Ronald M. Lanner1 Received: 22 August 2016 /Accepted: 14 December 2016 /Published online: 7 February 2017 # INRA and Springer-Verlag France 2017 Abstract which results from the interplay of genome, and environment & Key message Tree growth is driven by leaf primordium broadly construed. initiation at shoot apices through a series of growth and How then are primary and secondary growth initiated and developmental events largely mediated hormonally and controlled to yield the uniform product of each year’sgrowth often determinate in nature. This repeating pattern keeps cycle? What provides the stimulus that drives the growth of trees alive and reproductive and conserves the phenotype. apical and lateral meristems when internal and external con- ditions are conducive to biological activity? Keywords Morphogenesis . Shoot elongation . I propose here that the initiation of leaf primordia on shoot Photosynthesis . Xylogenesis . Phenotype conservation apical meristems that sets in motion the annual suite of tree growth activities. This may occur immediately or after a peri- od of dormancy. Once begun, those growth activities proceed to completion, unless prevented by disturbance or resource 1 Introduction depletion. The determinate nature of this synthesis does not exclude familiar sources of variability. Even determinate processes that are predictable in their outcome are influenced by envi- I have become increasingly convinced that this cycle is ronmental variation, historical events in a tree’s long develop- an entity so well integrated that it seems hardly possible mental time frame, and the unique genetic legacies of each to investigate or survey any of its parts successfully if taxon. Much of the supporting evidence cited below originat- they are separated from the whole (Sarvas 1974,p.3). ed from studies in Pinus because pines are the most studied of trees. Precise applicability to other taxa remains to be deter- Each year, a tree makes itself anew by adding modules of mined. The concept of leaf primordium initiation as a driving primary and secondary growth to the surface of the previous force for plant growth has been raised with regard to wheat ’ year s crown, stem, and roots. This deposition of new growth (Triticum aestivum L., Hay and Kemp 1990) but appears to be keeps the tree alive, as no tree can persist without renewing its a novel explanation for a complex woody plant. tissues. It also allows the tree to achieve a size and physiolog- ical stage of maturity that supports sexual reproduction. Moreover, it replicates the distinctive species phenotype, 2 Some supporting findings Handling Editor: Erwin Dreyer 2.1 Formation of stem units following primordium * Ronald M. Lanner initiation [email protected] Stem units are anatomically associated with leaves and pro- 1 Institute of Forest Genetics, Pacific Southwest Research Station, vide the organic connection between leaves and the stems USDA Forest Service, Placerville, CA, USA bearing them. 11 Page 2 of 7 Annals of Forest Science (2017) 74: 11 Atree’s first shoot apical meristem is that of its embryo, Within a class of similar shoots (e.g., same species, prove- and its first leaf primordia become the cotyledons (Foster and nance, age class, crown position, branch order), leaf-bearing Gifford 1974). Here, we focus on the shoot apical meristems stem units attain a rather uniform average length under normal that form subsequently and that comprise the expanding, then conditions. For example, MSUL was uniform throughout the declining, population of apical meristems active during a crowns of sapling red pine (Pinus resinosa Ait.) and eastern tree’s lifetime. white pine (Pinus strobus L.), though larger, older red pines Primordia are initiated by local cell division and enlarge- showed a gradient, with shorter stem units in the lower ment on the shoot apical meristem (Wardlaw 1968). New branches (Lanner 1968). Buckbee (1977), however, found primordia form successively above the last initiated, in the an inverse relationship between MSUL of lateral branches phyllotaxy characteristic of the taxon. Most will become em- and height in the crowns of subalpine firs (Abies lasiocarpa bryonic leaves or scales which will overwinter, in many spe- [Hook.] Nutt). The leaders of suppressed eastern white pines cies of temperate regions, within a bud. They will mature in had shorter and fewer stem units than dominants (Lanner the next growing season as the bud elongates into a shoot. The 1968), as had those of lodgepole pines (P. contorta Dougl. shoot then lignifies, precluding its further elongation. ex Loud.) in stagnated thickets in British Columbia (Worrall The portion of shoot associated with a leaf or scale is a stem et al.1985). unit defined by Doak (1935)inpinesas“an internode, togeth- Stem unit length can be affected by dominance relation- er with the node and nodal appendages at its distal extremity”; ships within a tree. Thus, Little (1970) found that when some thus a portion of shoot, the scale at its upper end, and the elongating shoots were removed from eastern white pine needle fascicle in the axil of that scale. An internode per se whorls, the remaining shoots exhibited increased (“compen- comprises that part of a stem between points of attachment of satory”) growth. As stem unit number in eastern white pine is successive leaves (nodes), but it does not include the leaf predetermined in year n, the added growth presumably result- itself. The term “internode” is ambiguous because it has tra- ed from increased stem unit length. In leaders of slash pine ditionally been used in forestry to denote that part of a stem saplings (Pinus elliottii Engelm.), MSUL of first summer between successive branch whorls, and alternative nomencla- shoots exceeded those of spring shoots and of second summer tures have been proposed to remedy the resulting confusion shoots (Lanner 1978). (Critchfield 1985, Powell 2009). In Great Basin bristlecone pine (Pinus longaeva D. K. Stem units can be measured by counting those on a shoot Bailey), neither shoot length, stem unit number, nor stem unit segment of known length to obtain the mean stem unit length length showed a consistent trend when regressed on tree age (MSUL). Young leaves produce plant growth regulators (Connor and Lanner 1989). Therefore, aging in these trees (PGRs) that induce vascular tissues in the immediately subja- cannot be defined in terms of diminishing annual shoot cent stem (Aloni 2013). These form leaf-bearing stem units growth. that can be regarded as the major building blocks of the young Stem unit characteristics may affect tree form. Subalpine fir woody shoot. leaders bore stem units “by far the longest in the tree,” which In bud-forming temperate-zone trees, stem units are typi- Buckbee (1977) suggested accounts in part for the distinctive cally initiated within buds in the year “n”, and the bud elon- spirelike form of the species. On the other hand, Lanner gates into a shoot in “n +1” (Lanner 1968). The number of (1989) attributed the umbrella crown of Italian stone pine stem units formed in a bud depends on how rapidly each forms (P. pinea L.) to consistently longer stem units in the lateral (the plastochron) and for how long the process continues shoots of its whorls than in the leaders of those whorls, despite (Cannell and Willett 1975). the leaders having more of them. The thinner crown of eastern white pine, compared to the 2.2 Properties of stem units denser red pine, may be due to white pine’smuchlongerstem units (e.g., 2.88–3.68 mm vs.1.07–1.08 mm) in 12-year-old When a pine bud elongates in the spring, its stem units start to trees (Lanner 1968). Great Basin bristlecone pine and its close grow almost simultaneously. Growth cessation however pro- relatives are easily identified by the “tasseled” appearance of ceeds from the base of the growing shoot upwards. The most its branches due to its exceptionally short needles and close- proximal and distal stem units grow to about 2× the length spaced fascicled stem units. they held in the dormant bud. The leaf-bearing stem units, Provenance has a role in stem unit length and number. In a which comprise most of the shoot’s length, elongate to as study of Scots pine (Pinus sylvestris L.) from Germany, much as 10× their length in the dormant bud (Lanner 1968). Sweden, Finland, and a Belgian plantation, MSUL in Thus, a stem unit’s contribution to the overall growth of its Minnesota, Michigan, and Missouri plantings was 1.67, shoot depends on its location. The sequence of stem unit elon- 1.68, 1.59, and 1.64 mm, respectively (Lanner 1968). While gations and their final lengths may be partly responsible for these differences were trivial, the tallest provenance exceeded the ubiquitous sigmoid curve of shoot growth.
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