Independently Silencing Two Photosynthetic Proteins inNicotiana attenuataHas Different Effects on Herbivore Resistance  

Abstract

Insect attack frequently down-regulates photosynthetic proteins. To understand how this influences the plant-insect interaction, we transformed Nicotiana attenuata to independently silence ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCase) activase (RCA) and RuBPCase and selected lines whose photosynthetic capacity was similarly reduced. Decreases in plant growth mirrored the decreases in photosynthesis, but the effects on herbivore performance differed. Both generalist (Spodoptera littoralis) and specialist (Manduca sexta) larvae grew larger on RCA-silenced plants, which was consistent with decreased levels of trypsin protease inhibitors and diterpene glycosides and increased levels of RuBPCase, the larvae's main dietary protein.RCA-silenced plants were impaired in their attack-elicited jasmonate (JA)-isoleucine (Ile)/leucine levels, but RuBPCasesilenced plants were not, a deficiency that could not be restored by supplementation with Ile or attributed to lower transcript levels of JAR4/6, the key enzyme for JA-Ile conjugation. From these results, we infer that JA-Ile/leucine signaling and the herbivore resistance traits elicited by JA-Ile are influenced by adenylate charge, or more generally, carbon availability in RCAbut not RuBPCase-silenced plants. Growth of generalist larvae on RuBPCase-silenced plants did not differ from growth on empty vector controls, but the specialist larvae grew faster on RuBPCase-silenced plants, which suggests that the specialist can better tolerate the protein deficiency resulting from RuBPCase silencing than the generalist can. We conclude that the plantherbivore interaction is more influenced by the particular mechanisms that reduce photosynthetic capacity after herbivore attack than by the magnitude of the decrease, which highlights the value of understanding defense mechanisms in evaluating growth-defense tradeoffs.An herbivore-attacked plant is known to reduce its photosynthetic capacity while increasing the production and accumulation of defense-related compounds (Walling, 2000;Hermsmeier et al., 2001;Kessler and Baldwin, 2002;Hahlbrock et al., 2003). In response to attack, plants must grow rapidly to compete and simultaneously maintain the defenses necessary to survive in environments with herbivores (Herms and Mattson, 1992). The dramatic up-regulation of defense metabolites likely requires metabolic adjustments in plant growth and reproduction (Halitschke et al., 2003;Reymond et al., 2004;Ralph et al., 2006). However, reductions in plant growth can also be understood as part of a plant's defense strategy, as reduced growth limits the availability of food and nutrition for the feeding insect (Hermsmeier et al., 2001;Hahlbrock et al., 2003). Allocating resources for resistance mechanisms is believed to reduce the availability of resources for growth; hence, resistance is thought to be costly in terms of plant growth and fitness (Heil and Baldwin, 2002). However, very little is known about how plants optimize their resource allocation when attacked by herbivores. Plan...

The Role of Arabidopsis Rubisco Activase in Jasmonate-Induced Leaf Senescence

“…Consistent with our data, it has been reported that the tobacco (Nicotiana tabacum) RCA gene was involved in herbivore resistance (Giri et al, 2006;Mitra and Baldwin, 2008). The tobacco RCA was decreased at the levels of transcript and protein abundance by herbivore damage (Giri et al, 2006).…”

“…The tobacco RCA was decreased at the levels of transcript and protein abundance by herbivore damage (Giri et al, 2006). Furthermore, down-regulation of this RCA gene caused reduced defense against herbivore attack (Mitra and Baldwin, 2008).…”

New perspective of jasmonate function in leaf senescence

“…[15][16][17][18][19][20][21] The rca-1 and rca-2 mutants displayed obviously decrease in the JA-induced expression of two defense-responsive genes plant defensin 1.2 (PDF1.2) and thionin 2.1 (Thi2.1), 5,22,23 suggesting that RCA may also play a role in JA-mediated defense responses. The multi-function of RCA in defense responses indicates that there might be some common elements in these processes, which is worthy to be identified.…”

Phloem Feeding Insect Stress and Photosynthetic Gene Expression

“…Silencing of these genes improved the performance of a native generalist (Spodoptera littoralis) and specialist (Manduca sexta) herbivorous larvae on transformed host plants (Mitra & Baldwin, 2008). Similarly, it was shown that independent silencing of the TMP 14 kDa thylakoid membrane phosphoprotein, PSI P700 apoprotein, and Fructose-1,6-bisphosphatase in near-isogenic (NILs) Triticum aestivum lines using VIGS, also affected host resistance to Diuraphis noxia in varying degrees (Jackson, 2010).…”

“…The linkage between photosynthesis and host defence was recently demonstrated by silencing two central photosynthetic proteins, i.e., ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase in Nicotiana attenuata using virusinduced gene silencing (VIGS) (Mitra & Baldwin, 2008). Silencing of these genes improved the performance of a native generalist (Spodoptera littoralis) and specialist (Manduca sexta) herbivorous larvae on transformed host plants (Mitra & Baldwin, 2008).…”