For almost a century the plant hormone auxin has been central to theories on apical dominance, whereby the growing shoot tip suppresses the growth of the axillary buds below. According to the classic model, the auxin indole-3-acetic acid is produced in the shoot tip and transported down the stem, where it inhibits bud growth. We report here that the initiation of bud growth after shoot tip loss cannot be dependent on apical auxin supply because we observe bud release up to 24 h before changes in auxin content in the adjacent stem. After the loss of the shoot tip, sugars are rapidly redistributed over large distances and accumulate in axillary buds within a timeframe that correlates with bud release. Moreover, artificially increasing sucrose levels in plants represses the expression of BRANCHED1 (BRC1), the key transcriptional regulator responsible for maintaining bud dormancy, and results in rapid bud release. An enhancement in sugar supply is both necessary and sufficient for suppressed buds to be released from apical dominance. Our data support a theory of apical dominance whereby the shoot tip’s strong demand for sugars inhibits axillary bud outgrowth by limiting the amount of sugar translocated to those buds. Significance It is commonly accepted that the plant hormone auxin mediates apical dominance. However, we have discovered that apical dominance strongly correlates with sugar availability and not apically supplied auxin. We have revealed that apical dominance is predominantly controlled by the shoot tip’s intense demand for sugars, which limits sugar availability to the axillary buds. These findings overturn a long-standing hypothesis on apical dominance and encourage us to reevaluate the relationship between hormones and sugars in this and other aspects of plant development.

Summary: Here, we tested whether rapid changes in carbohydrate transport and partitioning to storage organs would be induced by jasmonic acid (JA), a plant‐produced signal of herbivore attack known to induce resistance. Carbon‐11, introduced as¹¹CO₂, was used to track real‐time carbohydrate transport and partitioning nondestructively inPopulusspecies before and 12 h after application of JA to a single leaf. Jasmonic acid resulted in more rapid [¹¹C]‐photosynthate export from both local and systemic leaves, as well as greater partitioning of [¹¹C]‐photosynthate to the stem and roots. InPopulus tremuloides, following JA treatment, leaf starch decreased, but there was no change in photosynthetic rates or leaf soluble sugar concentration, indicating that recent photosynthate was diverted from starch accumulation in the leaf to other plant organs. Increasing the supply of photosynthate to roots and stems may shield resources from folivorous predators, and may also facilitate both storage and nutrient uptake, and ultimately lead to greater tolerance, either by enhancing regrowth capacity or by replacing nutrients consumed by herbivores.

Long distance transport in plants occurs in sieve tubes of the phloem. The pressure flow hypothesis introduced by Ernst Münch in 1930 describes a mechanism of osmotically generated pressure differentials that are supposed to drive the movement of sugars and other solutes in the phloem, but this hypothesis has long faced major challenges. The key issue is whether the conductance of sieve tubes, including sieve plate pores, is sufficient to allow pressure flow. We show that with increasing distance between source and sink, sieve tube conductivity and turgor increases dramatically in Ipomoea nil. Our results provide strong support for the Münch hypothesis, while providing new tools for the investigation of one of the least understood plant tissues.

Salicylic acid (SA) has long been implicated in plant responses to oxidative stress. SA overproduction in Arabidopsis thaliana leads to dwarfism, making in planta assessment of SA effects difficult in this model system. We report that transgenic Populus tremula × alba expressing a bacterial SA synthase hyperaccumulated SA and SA conjugates without negative growth consequences. In the absence of stress, endogenously elevated SA elicited widespread metabolic and transcriptional changes that resembled those of wild-type plants exposed to oxidative stress-promoting heat treatments. Potential signaling and oxidative stress markers azelaic and gluconic acids as well as antioxidant chlorogenic acids were strongly coregulated with SA, while soluble sugars and other phenylpropanoids were inversely correlated. Photosynthetic responses to heat were attenuated in SA-overproducing plants. Network analysis identified potential drivers of SA-mediated transcriptome rewiring, including receptor-like kinases and WRKY transcription factors. Orthologs of Arabidopsis SA signaling components NON-EXPRESSOR OF PATHOGENESIS-RELATED GENES1 and thioredoxins were not represented. However, all members of the expanded Populus nucleoredoxin-1 family exhibited increased expression and increased network connectivity in SA-overproducing Populus, suggesting a previously undescribed role in SA-mediated redox regulation. The SA response in Populus involved a reprogramming of carbon uptake and partitioning during stress that is compatible with constitutive chemical defense and sustained growth, contrasting with the SA response in Arabidopsis, which is transient and compromises growth if sustained.