Protein storage and root:shoot reallocation provide tolerance to damage in a hybrid willow system

Abstract

To determine the mechanistic basis of tolerance, we evaluated six candidate traits for tolerance to damage using F(2) interspecific hybrids in a willow hybrid system. A distinction was made between reproductive tolerance and biomass tolerance; reproductive tolerance was designated as a plant's proportional change in catkin production following damage, while biomass tolerance referred to a plant's proportional change in biomass (i.e., regrowth) following damage. F(2) hybrids were generated to increase variation and independence among candidate traits. Using three clonally identical individuals, pre-damage candidate traits for tolerance to damage (root:shoot ratio, total nonstructural carbohydrate, and total available protein) and post-damage candidate traits (relative root:shoot ratio, phenolic ratio, and specific leaf area ratio) were measured. The range of variation for these six candidate traits was broad. Biomass was significantly increased two years after 50% shoot length removal, and catkin production was not significantly reduced when damaged, suggesting that F(2) hybrids had great biomass tolerance and reproductive tolerance. Based on multiple regression methods, increased reproductive tolerance was associated with increased protein storage and decreased relative root:shoot ratio (reduced root allocation after damage). In addition, a positive relationship between biomass tolerance and condensed tannins was detected, and both traits were associated with increased reproductive tolerance. These four factors explained 57% of the variance in the reproductive tolerance of F(2) hybrids, but biomass tolerance explained the majority of the variance in reproductive tolerance. Changes in plant architecture in response to plant damage may be the underlying mechanism that explains biomass tolerance.

Tolerance and growth responses of populus hybrids and their genetically modified varieties to simulated leaf damage and harvest

“…Leaf damage can also increase the photosynthetic efficiency of plant tissue (Thomson et al, 2003;Stevens et al, 2008) suggesting that the loss of photosynthetic tissue in damaged portions of the plant may be additively beneficial to the undamaged portions as these plant parts will benefit from increases in both photosynthetic capacity and light radiation. Further, storage of proteins and carbohydrates may also function as tolerance mechanisms (Myers and Kitajima, 2007;Babst et al, 2008;Hochwender et al, 2011). For example, damaging insects may induce transport responses of carbon within woody plants (Babst et al, 2008) which potentially could induce rapid growth in remaining plant tissue.…”

“…Mechanisms mediating tolerance may be many; e.g. patterns in resource allocation (Canham et al, 1999;Eyles et al, 2009) and storage (Myers and Kitajima, 2007;Babst et al, 2008;Hochwender et al, 2011), photosynthetic activity (Thomson et al, 2003), phenology and plant architecture (Fornoni, 2011) and the mechanism through which tolerance is expressed may also vary with the type of damage received (the identity of the damaging herbivore). For example, removal of photosynthetic tissue may be compensated through increased photosynthetic ability of remaining tissue whereas when subjected to loss of woody biomass the plant may depend more on a resource storage mechanism (Marquis, 1996).…”

Resource availability and repeated defoliation mediate compensatory growth in trembling aspen (Populus tremuloides) seedlings

“…This may also indicate that both growth and reserves suffer from resource limitation. In parallel, earlier studies similarly reported that defoliation can influence the mobilization and storage of NSC between sinks and sources depending on resource availability (Babst et al, 2008; Schwachtje et al, 2005; Hochwender et al, 2012). However, our results contradict the results of Rivera-Solís et al (2012) who found higher carbon accumulation in roots of defoliated Ruellia nudiflora –a perennial herb–relative to non-defoliated plants.…”

“…We interpreted the large differences in root biomass between control and defoliated seedlings in a resource limited environment as a result of two main co-occurring processes: (a) after defoliation, translocation of photoassimilates from foliage to roots is severely reduced, which in turn reduces root growth, and (b) as new stem buds are activated to produce new leaves, roots translocate reserves to promote active growth in these carbohydrate sinks, which further compromises root growth. These predictions are based on the assumption that defoliation alters resource allocation in woody plants (Babst et al, 2008; Stevens, Kruger & Lindroth, 2008; Najar et al, 2014) and resources are utilized for growth of remaining plant tissues, particularly leaves (Landhäusser & Lieffers, 2002; Babst et al, 2008; Hochwender et al, 2012). Furthermore, substantial allocation of resources to roots may not be advantageous to early successional tree species–like aspen, because increasing above ground biomass, such as leaves and stems, may improve aspen’s competitive ability to capture lights.…”

“…Since we did not measure NSC concentrations in stems, we do not know how this could affect our conclusions. However, regardless of study systems, reserves can potentially serve to compensate for herbivore damage in plants (Babst et al, 2008; Schwachtje et al, 2005; Stevens, Kruger & Lindroth, 2008; Hochwender et al, 2012). …”